Comparison of Translocation and Transformation from Soil to Rice and

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Comparison of Translocation and Transformation from Soil to Rice and Metabolism in Rats for Four Arsenic Species Xu Wang, Anjing Geng, Yan Dong, Chongyun Fu, Hanmin Li, Yarong Zhao, Qing X. Li, and Fuhua Wang J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.7b01779 • Publication Date (Web): 01 Sep 2017 Downloaded from http://pubs.acs.org on September 1, 2017

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Journal of Agricultural and Food Chemistry

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Manuscript revised according to editor’s and reviewers’ comments for possible publication in

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Comparison of Translocation and Transformation from Soil to Rice and

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Metabolism in Rats for Four Arsenic Species

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Xu Wang,1,2,4 Anjing Geng,1,3#Yan Dong,5Chongyun Fu,6HanminLi,3Yarong Zhao,4Qing X.

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Li,2Fuhua Wang1,4*

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1. Public Monitoring Center for Agro-Product, Guangdong Academy of Agricultural Sciences,

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Guangzhou 510640, China; 2. Department of Molecular Biosciences and Bioengineering, University of Hawaii at Manoa, Honolulu, Hawaii 96822, USA; 3.Research Center for Trace Elements (Guangzhou) of Huazhong Agricultural University, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China; 4.Key Laboratory of Testing and Evaluation for Agro-product Safety and Quality, Ministry of Agriculture, Guangzhou 510640, China; 5. Department ofImmunology, Institute of Clinical Pharmacology, Guangzhou University of Chinese Medicine, Guangzhou 510405, China 6. Rice Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China.

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Version: August 30, 2017

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Corresponding author：：Fuhua Wang，e-mail:[email protected].

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ACS Paragon Plus Environment


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Abstract

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Arsenic (As) is ubiquitously present in the environment. The toxicity of As is related to

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its forms. This study was described to compare the translocation and transformation of four As

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species from soil to rice, and metabolism in rats for four arsenic species. A set of 26550 data

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was obtained from pot experiments of rice plants grown in soil fortified with four As species

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and 4050 data were obtained from rat experiments 81 rats administered with the four As species.

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The total As in grain from the methyl arsenate fortified soil was 6.1, 4.9, and 5.2 times of that

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from As(III)-, As(V)-, and dimethyl arsenate-fortified soil, respectively. The total As in husk

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was 1.2-7.8 times greater than that in grain. After oral administration each As species to rats,

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83-96% was accumulatively secreted via feces and urine, while 0.1-16% was detected in blood.

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The translocation, transformation and metabolism of different forms of arsenic are vary greatly.

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Key words: Arsenic; Translocation; Transformation; Metabolism

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Introduction Arsenic (As) is ubiquitous in the nature(1, 2). The concentrations of As in groundwater

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and soil often exceeded the maximum advisory in Argentina, Australia, Bangladesh, Chile,

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China, Hungary, India, Mexico, Peru, Thailand, and USA(3).It is highly bioaccumulative and

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toxicto humans and wildlife (4).Consumption of As-contaminated rice is amajor pathway of

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human exposure to As(5).Arsenate (As(V)) and arsenite (As(III)) are the main forms of inorganic

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arsenic, while methyl arsenate (MMAV)and dimethyl arsenate (DMAV) are the predominant 2


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species of organic arsenic.As(V) and As(III)in soil is mainly from contaminated groundwater,

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while pentavalent methylated As species such as MMAV and DMAV in soil come from

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pesticides, herbicides, additives to animal feeds, pharmaceutical products, and methylation of As

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by soil microorganisms or algae.

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Rice and water were more important to human total As intake than vegetables, pulses,

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and spices(6). Daily consumption of rice with a total As level was equivalent to the drinking

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water in Bangladesh (7, 8). The toxicity of As depends on its forms. In general, inorganic As is

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more toxic than organic As according to half lethal dose (LD50)values(9).Concern of As

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speciation in rice has been raised. The survey found that the main As species detected in the rice

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grains were As(III), DMAV, and As(V) in Europe, Bangladeshi, India, Australia, and USA

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(10-13). Organic brown rice syrup contained high concentrations of As(III), As(V)and

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DMAV(11). A number of cultivars with low grain As were identified from 76 cultivars of rice

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(14).Exposure assessment and measures for how to reduce arsenic intake were extensively

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studied, however, how As species are transferred and conversed from soil to rice and the adverse

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effects of As species require further in-depth study(15).

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A high priority has been placed on understanding environmental As mobility, toxicity,

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and bioavailability since 1970’s. Much research effort has been made on As(V)and As(III) which

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are the dominant forms in aerobic and flooded soils, respectively(16). Uptake and translocation

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of As to rice root is a major concern of route of exposure to As(17).Inorganic As transport into

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plant cells has been well studied(18).As(V) is taken up by phosphate transporters in plant(19).

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As(III) can transport by rice roots through two silicon transporters, Lsi1 (the aquaporin NIP2;1) 3



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and Lsi2 (an efflux carrier)(20). A short-term experiment demonstrated that As(V) uptake was

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strongly suppressed in the presence of phosphate, whereas As(III) transport was not affected by

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phosphate. There was a hyperbolic uptake of MMAV, and limited uptake of DMAV in the

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presence of phosphate(21). Uptake of MMAV and DMAV induckweed was also different from

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that of As(V)(10, 22). The mechanism of MMAV and DMAV uptake remains unknown and

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requires further research(23). The uptake behavior of MMAV and DMAV can be compared

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between them and with inorganic As if they are studied with inorganic As together under

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consistent conditions.

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It is well known that inorganic As are toxic to animals (24, 25). There is evidence for

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relationship between inorganic As exposure and liver cancer, diabetes, skin lesion, prostate

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cancer (26-29). Methylation is the primary metabolic pathway of ingested inorganic As (30, 31).

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Inorganic As is methylated to MMAV, which is reduced to monomethylarsonous acid (MMAIII).

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MMAIII is then methylated to DMAV, a small amount of which is then reduced to

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dimethylarsinous acid (DMAIII)(32, 33). MMAV and DMAV are more water soluble and more

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readily excreted from animal body (34, 35). MMAIII is much more toxic in vitro than its

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pentavalent form. MMAIII is however highly unstable and rapidly oxidized to MMAV, which

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makes it difficult to measure MMAIII in field studies (36). Methlytransferases have been

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purified from liver enzymes of the rabbit and the rhesus monkey. Inorganic As exposure

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increased prostate cancer cell viability(37). Bioavailability of As from contaminated soils to

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swine and mice were compared (1). Much study has been focused on inorganic As, whereas

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organic As are less well studied. Detailed research are needed to understand relationships 4


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between organic As and animal health (38). The bioavailability, transfer and conversion of As are affected by many factors, such as

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chemical properties of soil, variety of rice, microorganisms in soil and animals(39). That will be

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comparable if inorganic and organic As are studied together under consistent conditions. The

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objectives of this study were therefore to compare the transformation, uptake, translocation and

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bioaccumulation of As(V), As(III), MMAV and DMAV in rice plants and grain, as well as in

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rats. The present study utilized 300 pots of rice plants, five rice varieties, and five

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concentrations of four As species individually fortified in soil. A set of 22500 data was

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collected from As(V), As(III), MMAV, DMAV and total As in root, stem, leaf, husk and grain.

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In addition, 4050 data were obtained from rat experiments to compare the absorption,

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distribution, biotransformation, and excretion of As(V), As(III), MMAV and DMAV in rats.

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Materials and Methods

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Chemical reagents. As(V) (Na2HAsO4·7H2O) and DMAV [(CH3)2AsO2Na] were obtained

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from Sigma (St.Louis,MO, USA). As(III) (NaAsO2) and MMAV (CH3AsO3HNa·1.5H2O) were

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obtained from Chem Service (West Chester, PA, USA). Stock solutions (1,000mg As/L) were

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prepared by dissolving appropriate amounts of the arsenic compounds in 10mMHCl,stored in

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the dark at -4°C and were diluted with ultrapure water when standard solutions were needed.

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Total As reference materialGBW07602 was obtained from the National Standard Materials

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Center of China (Beijing). Ultrapure water (18.3MΩ·cm) was obtained by an Easy pure

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treatment system (Dubuque,Iowa,USA). HPLC grade methanol (J.T.Baker, USA) was used. 5



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Both high-purity (≥99.99%) argon (Ar) and nitrogen (N2) were purchased from Global

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Companyof China. Other reagents were analytical reagent grade.

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Soil, ricevariety, and plant growth. Soil was collected from a paddy field of Guangdong

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Academy of Agricultural Sciences(GAAS), China (23°09′28.31″N, 113°21′35.07″E).The soil

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was reddish brown late rite with pH 7.62.It contained 2.34%of organic matter content, 67.8

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mg/kg nitrogen (N),95.7 mg/kg phosphorus(P)and, 353 mg/kg pot assium(K), 6.21 mg/kg

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As,0.402 mg/kg cadmium(Cd),16.7 mg/kg chromium (Cr),39.4 mg/kg lead(Pb) and 0.112 mg/kg

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mercury(Hg).The soil was air-dried, crushed to pass 2mm sieve, and placed 7.0 kg into each pot

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(with no perforation, 24.5 x 21.1 x29.0 cm).

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Five varieties were Yuejingsimiao 2 (YJS), Tianyou 116 (TY), Tianfeng B (TF), Black

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kernelled rice (BK), and Guanghui 116 (GH), which were obtained from Rice Research Institute

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of GAAS, China. YJS and BK were inbred rice variety. TY was hybrid rice variety. TF and GH

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were the female parent and male parent of TY, respectively.

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Thirty-day-old seedlings of each rice variety were transplanted in 60 pots (60 x 5

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varieties). After 7 days, the transplanted seedlings revived. The solutions of As(III), As(V),

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MMAV and DMAV were supplied to separately contaminate soils in pots. The As solutions

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were diluted with distilled water and make the final volume of 2L according to the fortification

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concentrations. The fortified solutions were poured evenly into the pots after transplanted

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seedlings revived. Fifteen pots of each paddy variety were contaminated by each As species at

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concentrations of 0, 50, 100, 150, and 200 mg As/ kg in triplicate (5concentrations x 3).Pots 6


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were flooded with ultrapure water at 3–4 cm water depth.

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Rat, diets, husbandry, and As administration. 81 SPF SD male rats in 180±20g and their rodent

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diet were purchased from the Experimental Animal Center of Guangzhou University of Chinese

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Medicine under the permit number SCXK (Yue) 2013-0034 (No.44005800001963).

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All animal experiments were approved by the Experimental Animal Center of

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Guangzhou University of Chinese Medicine and performed in compliance with the regulation

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of Animals Welfare Act of the U.S. Department of Agriculture. All animals were raised under

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controlled temperature (22 ± 2 °C) and light (12 h light/12 h darkness) with air circulation,

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fresh water and animal food. Nine groups of rats consisted of one control group, 4 low dose

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groups (daily 0.875 mg As/kg body weight (bw)), and 4 high dose groups (daily 1.750 mg

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As/kg bw) of As(III), As(V), MMAV and DMAV(9 rats x 9 groups). Treated rats were weighed

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daily and were orally gavaged with1mLof As solution per 200g bw, but the controlgroupwith

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water alone.

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Sample collection. Rice plant samples were collected in the seedlings stage [30th day after

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treatment (DAT)], grain-filling stage (55thDAT) and harvest stage (70thDAT). The plants were

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divided into roots, stems, leaves and grains (except seedlings stage). Grains from rice plants

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grown in 200 mg As/kg soil except As(V) were not collected because of no grains. They were

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cut into pieces and ground with dry ice separately. The prepared samples were stored at -18°C

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until As analysis. 7



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Rats were housed in metabolism cages to collect and weigh the urine and feces. The

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urine and feces were separately combined for the analysis of total As and As species. The

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animals were not given any feeds and water for 12 h after they were gavaged at days 1, 14 and

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28. Urine and feces samples were collected after 8 h, and orbital venous blood were collected

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after 12 h. After blood collection, food and drink were provided normally. Urine, feces and

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orbital venous blood were stored at -18°C until As analysis. Rats were executed by cervical

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dislocation, followed by separation of heart, brain, livers, lungs, spleen, kidneys and muscles

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for weight. The separated tissue samples were smashed in a homogenizer for As content

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measurements.

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Total As and As species determination. Total As content were determined on a hydride

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generation-atomic fluorescence spectrometer (HG-AFS, Jitian Beijing) after plant and animal

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samples were digested with a mixture of equal volume concentrated HNO3, H2SO4 and HClO4.

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The reference material GBW07602was used for the quality control.

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Half grams of animal and plant samples were weighed in 50-mL centrifuge tubes,

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followed by addition of 10mL of 50% aqueous methanol. After ultrasound assisted extraction

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for 30min, the samples were centrifuged at12750g for 10min at 4°C. The supernatant was

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filtered through a 0.22µm PET filter. As(III), As(V), MMAV and DMAV in the filtrates were

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measured on a HPLC-ICP-MS spectrometer (Agilent Technologies, USA) connected with a

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Hamilton PRP X-100 column (250 x 4.1 mm). The mobile phase was 20 mm

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(NH4)2HPO4aqueous solution at pH 6.0 and was set at a constant flow rate of 1.25mL/min. The 8


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MS conditions were the same as described by Abedin et al. (21, 40).

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Statistical analysis. Rice and rat data were means ± standard deviations of three and six

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replications, respectively. All data were measured on fresh weight basis. Analysis of variance

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(ANOVA) with Least Significance Difference (LSD) was performed with SPSS (v13.0, IBM

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Co., USA).Curve fitting was done with Sigma Plot (Jandel Scientific, Erkrath, Germany).

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Results

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As in rice plants. After the rice plants were fortified with 50, 100, 150, and 200 mg As/kg soil,

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three types of rice plants died approximately 4-6 weeks after applications of As(III) or As(V)at

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150 mg/kg or greater.Rice plants in As(III) polluted soil died 2 weeks earlier than As(V). TY and

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YJS planted in 150 mg AS/kg MMAV added soil and TY planted in 200 mg AS/kg MMAV

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added soil had no earing and flowering when the others were harvested. No difference in rice

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plant growth was observed among the soils fortified with 50 mg/kg of As(III),As(V), DMAV and

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MMAV. To compare the behavior of the four As species, we chose the rice plant fortified with

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100 mg As/kg in the remainder study.

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Figure1 shows the content of As in rice husk and grain from 100 mg As/kg soil. As(III)

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detected in grain from As(V) and DMAV fortified soil constituted greater than 86.7% of total As,

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while MMAV in grain from MMAV fortified soil constituted about 71% of total As. The sum

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proportion of As (III) and DMAV, which grew from As (III) fortified soil were about 90% of

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total As detected. The total content of As was 1.01 ± 0.08, 0.346 ± 0.023, 2.18± 0.12, and 0.183 9



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± 0.011 mg/kg in husk from plants grown in soils fortified with As(III), As(V), MMAV and

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DMAV, respectively, while that correspondingly was0.130± 0.038, 0.162 ± 0.014, 0.788± 0.062,

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and 0.151 ± 0.013 mg/kg in grain. The sum content of As(III), As(V), MMAV and DMAV

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accounted for 98.3 ± 3.2% of total As, and therefore the four As species were further analyzed.

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The total As in husk was 7.8, 2.1, 2.8,and 1.2 times of that in grain from rice plants grown in

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soils fortified with As(III), As(V), MMAV, and DMAV, respectively. The total As in grain from

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the MMAV contaminated soil was 6.1, 4.9, and 5.2 times of that from As(III),As(V), and DMAV

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contaminated soil, respectively.

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Figures 2 and 3 show the distribution and content of As species in rice plants tissues,

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respectively. When rice plants grew in As(III)-fortified soil, all four As species were detected in

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roots, but three As species (As(III), As(V)and DMAV) were detected in stems, leaves and

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grains. As(III) content decreased in an order of root >leaf>husk> stem>grain, while As(V)

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content decreased in an order of stem >leaf >root >husk>grain. MMAV could not be detected

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except root of YJS variety. DMAV content was husk >> leaf > root > stem>grain. When rice

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plants grew in As(V) fortified soil, As(III) and As(V) were detected in all parts of rice, but

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MMAV and DMAV were not detected. The content of As(III) and As(V)followed an order of

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root > leaf >stem >husk>> grain. When rice plants grew in MMAV fortified soil, all four As

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species were all detected in each part of rice plants. As(III) content decreased from root, leaf,

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husk, stem to grain, whereas As(V) content decreased from root, stem, leaf, husk to grain.

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MMAV content was root > stem > leaf >husk > grain, whereas DMAV content was opposite.

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When rice plants grew in DMAV fortified soil, As(III)and DMAV were detected in all plant 10


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parts, but As(V) and MMAV were not detected. The As(III) content was very low(stem>leaf>husk >grain.

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Relation of As species between soil and rice. Linear correlations between As in rice grain and

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soil were found as follows: As(III) in grain = 0.0027As(V) in soil + 0.0136, R² = 0.984; MMAV

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in grain = 0.0347 MMAV in soil - 0.2233,R² = 0.986; As(III) in grain = 0.0024 DMAV in soil -

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0.02, R² = 0.964. Multiple linear positive correlations were found for the cases below: As(V) in

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grain = 4E-05(As(III) in soil)2 - 0.0014 As(III) in soil + 0.0057, R² = 0.998; DMAV in grain =

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3E-05(As(III)in soil)2 - 0.0008 As(III)in soil + 0.0012, R² = 1.00; As(V) in grain = 4E-06(As(V)

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in soil)2 - 0.0003 As(V) in soil + 0.003, R² = 0.961; DMAV in grain= 8E-06(DMAV in soil)2-

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0.0005 DMAV in soil + 0.0011, R² = 0.997.Other correlations were also found as follows: As(III)

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in grain = -2E-05(As(III)in soil)2 + 0.0054 As(III)in soil - 0.0229, R² = 0.921; As(III)in grain=

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-6E-05(MMAV in soil)2 + 0.011 MMAV in soil - 0.035, R² = 0.838; As(V) in grain =

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-2E-05(MMAV in soil)2 + 0.0041 MMAV in soil - 0.022, R² = 0.767; DMAV in grain =

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-2E-05(MMAV in soil)2 + 0.0047 MMAV in soil - 0.0044, R² = 0.992.

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As distribution in rats.Figure4showsdistribution of As species in 8 rat organ tissues, urine and

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feces after 28 days of gavage administration. DMAV was detected in all rat organ samples after

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rats were administered with a low and high dose of As(III), As(V), and MMAV, except no

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DMAV detected in kidney at the low dose of As(III). Both DMAV and MMAV were detected in

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urine and feces in rats administered with a low and high dose of As(III), As(V), and MMAV. In 11



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addition, As(III) was detected in feces from As(III) exposed rats, while As(III) and As(V) were

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detected in feces from (As(V) exposed rats. However, only DMAV was detected in liver, blood,

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urine and feces rats exposed to DMAV.

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In general, blood As content in rats administered with As(III), As(V), and MMAV were

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approximately 4-1728 fold greater than the other samples. The blood DMAV concentration (58.1

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mg/L) in high dose As(III)rats was 43,10,17,11,7,60,63,390,and 1120 times greater than that in

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feces, urine, liver, lungs, spleen, kidney, heart, brain, and muscles, respectively (data not

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shown).The blood DMAV concentration (50.2 mg/L) in high dose As(V)rats was

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46,8,39,9,4,14,12,1728,and 880 times greater than that feces, urine, liver, lungs, spleen, kidney,

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heart, brain, and muscles, respectively. The blood DMAV in high dose MMAV rats (23.8 mg/L)

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was 7,10,114,25,43,30,6,189, and 554 times greater than feces, urine, liver, lungs, spleen, kidney,

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heart, brain, and muscles, respectively. DMAV content in feces, urine, blood, and liver from high

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dose DMAV rats were 3.37, 0.351, 0.344, and0.182 mg/L, respectively.

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Figure 5 shows the mass balance of As species between the amount administered and the

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amount of As species detected, which 82.9% of As(III), 85.1% of As(V), 95.0% of MMAV and

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96.2% of DMAV were excreted through urine and feces.73.2%, 65.7%,and 91.0% of the orally

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dosed As(III), As(V) and DMAV were excreted as DMAV in urine. 62.4% and 32.7%of the

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dosed MMAV excreted through, respectively, urine and feces as MMAV and DMAV. Blood

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contained 16.2%, 14.1%, 4.65%, and 0.120% of the dosed As(III), As(V),MMAV, and DMAV,

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respectively.

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Bioaccumulation and transformation of As species in rats. DMAV was detected in all feces

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except the first day feces. As the duration of intragastric administration of As(III), As(V) and

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MMAV increased, DMAV was primarily accumulated in urine and blood. However, most

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DMAV (96.2%) was directly secreted through urine and feces, but little DMAV was absorbed

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and distributed among organs.

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Discussion In the present study, we utilized 300 pots of rice plants, five rice varieties, and five

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concentrations of four As species individually fortified in soil. A set of 22500 data was obtained

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for As(V), As(III), MMAV, DMAV and total As in root, stem, leaf, husk and grain. In addition,

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4050 data were obtained from rat experiments to analysis the absorption, distribution,

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biotransformation, and excretion of As(V), As(III), MMAV and DMAV in rats.

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Cultivation of rice plants in soil fortified with As(III) caused detection of As(III), As(V),

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MMAV and DMAV in roots and As(III), As(V) and DMAV in stems, leaves and grains. When

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rice plants grew in As(V) fortified soil, As(III) was the dominant As species detected in rice

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plants and grains. When rice plants grew in MMAV fortified soil, all four As species were

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detected in each part of rice plants. DMAV was much less mobile for uptake and translocations.

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When rice plants grew in DMAV fortified soil, As(III) and DMAV were observed in all parts of

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rice plants, but not As(V) and MMAV. The total As content in grain from MMAV contaminated

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soil was 6.1, 4.9, 5.2 times greater than that from As(III),As(V) and DMAV contaminated soil,

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respectively. Abedin et al. (41) found that the concentration-dependent uptake of MMAV into 13



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rice roots can be described by Michaelis–Menten kinetics, whereas the DMA uptake did not fit

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either a Michaelis–Menten kinetics or a linear function. A later study by Andrew et al. showed

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that the DMA uptake into maize (Zea mays) roots can be described by a Michaelis–Menten plus

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linear function(42). Chemical and biological processes taking place in therhizosphere may

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influence the speciation of As and its bioavailability to plants. Uptake, translocations and

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concentration coefficients of As varied largely with forms of As species, indicating it is

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necessary to study both inorganic and organic As species.

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Rice plants died approximately 4-6 weeks after applications of As(III) or As(V) at 150

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mg/kg or greater. Rice plants in As(III) polluted soil died 2 weeks earlier than As(V). MMAV

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at 150 mg/kg in soil apparently stimulated rice biomass growth, but delayed the physiological

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development and caused no grains. It means, if the content of As in soil is greater than 150

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mg/kg, the rice would be physiologically poisoned before harming human health.

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The total content of As was 1.01, 0.34, 2.18, and 0.183 mg/kg in husk from plants grown

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in soils fortified with As(III), As(V), MMAV and DMAV, respectively, while that

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correspondingly was 0.130, 0.162, 0.788, and 0.151mg/kg in grain. The total As in husk was 7.8,

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2.1, 2.8,and 1.2 times of that in grain from rice plants grown in soils fortified with As(III), As(V),

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MMAV, and DMAV, respectively. The transfer of As from soil to grain was lower in

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comparison to husk, which makes rice grain safer(43). The total As in leaf and stem are much

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greater than grain, although As content in rice shoot, leaf and stem are not regulated by food

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hygiene regulations. Rice shoot, leaf and stem are used as cattle feed in many countries, in which

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As may be accumulated into cattle and thus increase As exposure to humans via food chain(44). 14


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According to risk assessment conducted by JECFA in 2010, BMDL0.5 of inorganic As is

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3.0 µg/kg bw per day from lung cancer epidemiological studies(45). If a 63 kg adult consumes

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238.3 g/d of rice (7), the total As level of 0.130, 0.162, 0.788, and 0.151 mg/kg in grain from

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plants grown in soils fortified with As(III), As(V), MMAV and DMAV, if all the total As is

301

inorganic As, the margin of exposure would equal 18%, 22%, 110%, and 21% of the BMDL0.5,

302

respectively. However, the result is under the hypothesis of total As is inorganic As conditions,

303

organic As will less risk. In addition, according to our result, MMAV in grain from MMAV

304

fortified soil constituted about 71% of total As, MMAV is much less toxic than As(III) and

305

As(V).

306

82.9% of As(III), 85.1% of As(V), 95.0% of MMAV and 96.2% of DMAV, each As

307

species orally dosed to rats, were excreted through feces and urine, more than 80% of the four

308

As species were excreted. The As left in the rat is mostly kept in the blood, 16.2% of As(III),

309

14.1% of As(V), 4.65% of MMAV and 0.120% of DMAV were detected in blood, and all of

310

the As species left in blood were as in the form of DMAV. Inorganic As and MMAV may be

311

methylated to DMAV in rats(46).

312

The bioavailability of As from soil to grain can be affected by many factors, such as

313

redox potential of soil, pH value of soil, flood, variety of rice (47). The soluble As content of soil

314

whose redox potential was 200 mV was 13-fold as compared to 500 mV. The concentration

315

coefficient of grain from plants in 10 mg As/kg soil of greenhouse was approximately 2.5%

316

under aerobic conditions. However, flooding can increase grain As content by 10-15 folds

317

relative to aerobically grown rice(48). Different rice varieties have different coefficient. The 15



318

mean concentration coefficient of total As from soil to grain was approximately 6.6% based on

319

the survey of 204 commercial rice samples purchased mostly in retail stores in upstate New York

320

and samples from Canada, France, Venezuela, and other countries(49, 50). As content in brown

321

rice was 1.5 and 2.8 fold higher than that in white rice and other rice, while As content in long

322

rice were 1.2 and 1.5 fold higher than that in white rice and other rice(14, 49).When rice plants

323

were irrigated with As-contaminated water in Bangladesh, the mean coefficient of total As was

324

0.4%(41). The mean coefficients of total As was 0.2-1.1%, while those of the four As species

325

varied from 0.2% to 6.6% in the present study(11). Large difference occurred due to not only soil

326

properties, rice varieties, but also microbial influences.

327 328

Acknowledgement This study was supported in part by the Dean fund of Guangdong Academy of

329 330

Agricultural Sciences. XW was a recipient of scholarship from Guangdong Academy of

331

Agricultural Sciences, China.

332 333

References

334 335 336 337 338 339 340 341 342

1.

Li, J.; Li, C.; Sun, H. J.; Juhasz, A. L.; Luo, J.; Li, H. B.; Ma, L. Q., Arsenic relative bioavailability in contaminated

soils: comparison of animal models, dosing schemes, and biological end points. Environmental Science & Technology 2016, 50, 453-461. 2.

Cheyns, K.; Waegeneers, N.; Van de Wiele, T.; Ruttens, A., Arsenic release from foodstuffs upon food

preparation. Journal of Agricultural and Food Chemistry 2017, 65, 2443-2453. 3.

Hernandez-Zavala, A.; Valenzuela, O. L.; Matousek, T.; Drobna, Z.; Dedina, J.; Garcia-Vargas, G. G.; Thomas, D.

J.; Del Razo, L. M.; Styblo, M., Speciation of arsenic in exfoliated urinary bladder epithelial cells from individuals exposed to arsenic in drinking water. Environmental Health Perspectives 2008, 116, 1656-1660. 4.

Bienert, G. P.; Thorsen, M.; Schussler, M. D.; Nilsson, H. R.; Wagner, A.; Tamas, M. J.; Jahn, T. P., A subgroup of 16


Page 16 of 27

Page 17 of 27

343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383


plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biology 2008, 6, 26. 5.

Williams, P. N.; Price, A. H.; Raab, A.; Hossain, S. A.; Feldmann, J.; Meharg, A. A., Variation in arsenic

speciation and concentration in paddy rice related to dietary exposure. Environmental Science & Technology 2005, 39, 5531-5540. 6.

Abedin, M. J.; Cotter-Howells, J.; Meharg, A. A., Arsenic uptake and accumulation in rice (Oriza sativa L.)

irrigated with contaminated water. Plant and Soil 2002, 240, 311-319. 7.

Li, X.; Xie, K.; Yue, B.; Gong, Y.; Shao, Y.; Shang, X.; Wu Y., Inorganic arsenic contamination of rice from

Chinese major rice-producing areas and exposure assessment in Chinese population. Science China Chemistry. 2015, 58(12), 1898-1905. 8.

Hettick, B. E.; Cañas-Carrell, J. E.; French, A. D.; Klein, D. M., Arsenic: a review of the element’s toxicity, plant

interactions, and potential methods of remediation. Journal of Agricultural and Food Chemistry 2015, 63, 7097-7107. 9.

Huang, Y.; Wang, M.; Mao, X.; Qian, Y.; Chen, T.; Zhang, Y., Concentrations of inorganic arsenic in milled rice

from China and associated dietary exposure assessment. Journal of Agricultural and Food Chemistry 2015, 63, 10838-10845. 10. Rahman, M. A.; Kadohashi, K.; Maki, T.; Hasegawa, H., Transport of DMAA and MMAA into rice (Oryza sativa L.) roots. Environmental and Experimental Botany 2011, 72, 41-46. 11. Jackson, B. P.; Taylor, V. F.; Karagas, M. R.; Punshon, T.; Cottingham, K. L., Arsenic, organic foods, and brown rice syrup. Environmental Health Perspectives 2012, 120, 623-626. 12. Rahman, M. A.; Rahman, M. M.; Reichman, S. M.; Lim, R. P.; Naidu, R., Arsenic speciation in australian-grown and imported rice on sale in australia:i mplications for human health risk. Journal of Agricultural and Food Chemistry 2014, 62, 6016-6024. 13. Awata, H.; Linder, S.; Mitchell, L. E.; Delclos, G. L., Association of dietary intake and biomarker levels of arsenic, cadmium, lead, and mercury among asian populations in the United States: NHANES 2011-2012. Environmental Health Perspectives 2017, 125, 314-323. 14. Norton, G. J.; Islam, M. R.; Deacon, C. M.; Zhao, F.-J.; Stroud, J. L.; McGrath, S. P.; Islam, S.; Jahiruddin, M.; Feldmann, J.; Price, A. H.; Meharg, A. A., Identification of Low Inorganic and Total Grain Arsenic Rice Cultivars from Bangladesh. Environmental Science & Technology 2009, 43, 6070-6075. 15. Carlin, D. J.; Naujokas, M. F.; Bradham, K. D.; Cowden, J.; Heacock, M.; Henry, H. F.; Lee, J. S.; Thomas, D. J.; Thompson, C.; Tokar, E. J.; Waalkes, M. P.; Birnbaum, L. S.; Suk, W. A., Arsenic and environmental health: state of the science and future research opportunities. Environmental Health Perspectives 2016, 124, 890-899. 16. M., J.; V., N.; B., R.; F., R.; M., R., Bioavailability of inorganic arsenic in cooked rice: practical aspects for human health risk assessments. Journal of Agricultural and Food Chemistry 2005, 53, 8829-8833. 17. Carlin, D. J.; Naujokas, M. F.; Bradham, K. D.; Cowden, J.; Heacock, M.; Henry, H. F.; Lee, J. S.; Thomas, D. J.; Thompson, C.; Tokar, E. J.; Waalkes, M. P.; Birnbaum, L. S.; Suk, W. A., Arsenic and environmental health: state of the science and future research opportunities. Environmental Health Perspectives 2015, 124, 890-899. 18. Tang, Z.; Lv, Y.; Chen, F.; Zhang, W.; Rosen, B. P.; Zhao, F. J., Arsenic methylation in arabidopsis thaliana expressing an algal arsenite methyltransferase gene increases arsenic phytotoxicity. Journal of Agricultural and Food Chemistry 2016, 64, 2674-2681. 19. Seyfferth, A. L.; Morris, A. H.; Gill, R.; Kearns, K. A.; Mann, J. N.; Paukett, M.; Leskanic, C., Soil incorporation 17



384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424

of silica-rich rice husk decreases inorganic arsenic in rice grain. Journal of Agricultural and Food Chemistry 2016, 64, 3760-3766. 20. Zhao, F. J.; Ma, J. F.; Meharg, A. A.; McGrath, S. P., Arsenic uptake and metabolism in plants. New Phytologist 2009, 181, 777-794. 21. Abedin, M. J.; Feldmann, J.; Meharg, A. A., Uptake kinetics of arsenic species in rice plants. Plant Physiology 2002, 128, 1120-1128. 22. Li, R. Y.; Ago, Y.; Liu, W. J.; Mitani, N.; Feldmann, J.; McGrath, S. P.; Ma, J. F.; Zhao, F. J., The rice aquaporin Lsi1 mediates uptake of methylated arsenic species. Plant Physiology 2009, 150, 2071-2080. 23. Tang, Z.; Lv, Y.; Chen, F.; Zhang, W.; Rosen, B. P.; Zhao, F. J., Arsenic Methylation in Arabidopsis thaliana Expressing an Algal Arsenite Methyltransferase Gene Increases Arsenic Phytotoxicity. Journal of Agricultural and Food Chemistry 2016, 64, 2674-2681. 24. Engstrom, K. S.; Vahter, M.; Fletcher, T.; Leonardi, G.; Goessler, W.; Gurzau, E.; Koppova, K.; Rudnai, P.; Kumar, R.; Broberg, K., Genetic variation in arsenic (+3 oxidation state) methyltransferase (AS3MT), arsenic metabolism and risk of basal cell carcinoma in a European population. Environmental and Molecular Mutagenesis 2015, 56, 60-69. 25. Howe, C. G.; Liu, X.; Hall, M. N.; Slavkovich, V.; Ilievski, V.; Parvez, F.; Siddique, A. B.; Shahriar, H.; Uddin, M. N.; Islam, T.; Graziano, J. H.; Costa, M.; Gamble, M. V., Associations between Blood and Urine Arsenic Concentrations and Global Levels of Post-Translational Histone Modifications in Bangladeshi Men and Women. Environmental Health Perspectives 2016, 124, 1234-1240. 26. Pierce, B. L.; Tong, L.; Argos, M.; Gao, J.; Farzana, J.; Roy, S.; Paul-Brutus, R.; Rahaman, R.; Rakibuz-Zaman, M.; Parvez, F.; Ahmed, A.; Quasem, I.; Hore, S. K.; Alam, S.; Islam, T.; Harjes, J.; Sarwar, G.; Slavkovich, V.; Gamble, M. V.; Chen, Y.; Yunus, M.; Rahman, M.; Baron, J. A.; Graziano, J. H.; Ahsan, H., Arsenic metabolism efficiency has a causal role in arsenic toxicity: Mendelian randomization and gene-environment interaction. International Journal of Rpidemiology 2013, 42, 1862-1871. 27. Martin, E.; Gonzalez-Horta, C.; Rager, J.; Bailey, K. A.; Sanchez-Ramirez, B.; Ballinas-Casarrubias, L.; Ishida, M. C.; Gutierrez-Torres, D. S.; Hernandez Ceron, R.; Viniegra Morales, D.; Baeza Terrazas, F. A.; Saunders, R. J.; Drobna, Z.; Mendez, M. A.; Buse, J. B.; Loomis, D.; Jia, W.; Garcia-Vargas, G. G.; Del Razo, L. M.; Styblo, M.; Fry, R., Metabolomic characteristics of arsenic-associated diabetes in a prospective cohort in Chihuahua, Mexico. Toxicological sciences : an official journal of the Society of Toxicology 2015, 144, 338-346. 28. Currier, J. M.; Ishida, M. C.; Gonzalez-Horta, C.; Sanchez-Ramirez, B.; Ballinas-Casarrubias, L.; Gutierrez-Torres, D. S.; Ceron, R. H.; Morales, D. V.; Terrazas, F. A.; Del Razo, L. M.; Garcia-Vargas, G. G.; Saunders, R. J.; Drobna, Z.; Fry, R. C.; Matousek, T.; Buse, J. B.; Mendez, M. A.; Loomis, D.; Styblo, M., Associations between arsenic species in exfoliated urothelial cells and prevalence of diabetes among residents of Chihuahua, Mexico. Environmental Health Perspectives 2014, 122, 1088-1094. 29. Benbrahim-Tallaa, L.; Waalkes, M. P., Inorganic arsenic and human prostate cancer. Environmental Health Perspectives 2008, 116, 158-164. 30. Lu, K.; Abo, R. P.; Schlieper, K. A.; Graffam, M. E.; Levine, S.; Wishnok, J. S.; Swenberg, J. A.; Tannenbaum, S. R.; Fox, J. G., Arsenic exposure perturbs the gut microbiome and its metabolic profile in mice: an integrated metagenomics and metabolomics analysis. Environmental Health Perspectives 2014, 122, 284-291. 31. Liu, Q.; Leslie, E. M.; Le, X. C., Accumulation and transport of roxarsone, arsenobetaine, and inorganic arsenic using the human immortalized Caco-2cell line. Journal of Agricultural and Food Chemistry 2016, 64, 8902-8908. 18


Page 18 of 27

Page 19 of 27

425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453 454 455 456 457 458 459 460 461 462 463 464 465


32. Melak, D.; Ferreccio, C.; Kalman, D.; Parra, R.; Acevedo, J.; Perez, L.; Cortes, S.; Smith, A. H.; Yuan, Y.; Liaw, J.; Steinmaus, C., Arsenic methylation and lung and bladder cancer in a case-control study in northern Chile. Toxicology and Applied Pharmacology 2014, 274, 225-231. 33. Schlebusch, C. M.; Lewis, C. M., Jr.; Vahter, M.; Engstrom, K.; Tito, R. Y.; Obregon-Tito, A. J.; Huerta, D.; Polo, S. I.; Medina, A. C.; Brutsaert, T. D.; Concha, G.; Jakobsson, M.; Broberg, K., Possible positive selection for an arsenic-protective haplotype in humans. Environmental Health Perspectives 2013, 121, 53-58. 34. Kozul, C. D.; Ely, K. H.; Enelow, R. I.; Hamilton, J. W., Low-dose arsenic compromises the immune response to influenza A infection in vivo. Environmental Health Perspectives 2009, 117, 1441-1447. 35. Yu, Z. M.; Dummer, T. J.; Adams, A.; Murimboh, J. D.; Parker, L., Relationship between drinking water and toenail arsenic concentrations among a cohort of Nova Scotians. Journal of Exposure Science & Environmental epidemiology 2014, 24, 135-144. 36. Kalman, D. A.; Dills, R. L.; Steinmaus, C.; Yunus, M.; Khan, A. F.; Prodhan, M. M.; Yuan, Y.; Smith, A. H., Occurrence of trivalent monomethyl arsenic and other urinary arsenic species in a highly exposed juvenile population in Bangladesh. Journal of Exposure Science & Environmental Epidemiology 2014, 24, 113-120. 37. Shearer, J. J.; Wold, E. A.; Umbaugh, C. S.; Lichti, C. F.; Nilsson, C. L.; Figueiredo, M. L., Inorganic arsenic related changes in the stromal tumor microenvironment in a prostate cancer cell-conditioned media model. Environmental Health Perspectives 2015, 1-34. 38. J., M. C., Influence of environmental exposure on human epigenetic regulation. Journal of Experimental Biology 2015, 218, 71-79. 39. Neumann, R. B.; Pracht, L. E.; Polizzotto, M. L.; Badruzzaman, A. B. M.; Ali, M. A., Biodegradable organic carbon in sediments of an arsenic-contaminated aquifer in Bangladesh. Environmental Science & Technology Letters 2014, 1, 221-225. 40. Qu, H.; Mudalige, T. K.; Linder, S. W., Arsenic speciation in rice by capillary electrophoresis/inductively coupled plasma mass spectrometry: enzyme-assisted water-phase microwave digestion. Journal of Agricultural and Food Chemistry 2015, 63, 3153-3160. 41. Abedin, M. J.; Cotter-Howells, J.; Meharg, A. A., Arsenic accumulation and metabolism in rice (Oryza sativa L.). Plant and Soil 2002, 240, 311-319. 42. A., M. A.; J., H.-W., Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytologist 2002, 154, 29–43. 43. S., R., Arsenic and paddy rice: a neglected cancer risk? Science New Series 2008, 321, 184-185. 44. Clemente, M. J.; Devesa, V.; Vélez, D., Dietary strategies to reduce the bioaccessibility of arsenic from food matrices. Journal of Agricultural and Food Chemistry 2016, 64, 923-931. 45. WHO Seventy-second meeting report of the joint FAOIWHO expert committee on food additives, summary and conclusions: Rome; World Health Organization: Rome, 2010. 46. Shen, S.; Li, X. F.; Cullen, W. R.; Weinfeld, M.; Le, X. C., Arsenic binding to proteins. Chemical Reviews 2013, 113, 7769-7792. 47. Polizzotto, M. L.; Birgand, F.; Badruzzaman, A. B. M.; Ali, M. A., Amending irrigation channels with jute-mesh structures to decrease arsenic loading to rice fields in Bangladesh. Ecological Engineering 2015, 74, 101-106. 48. Xu, X. Y.; Mcgrath, S. P.; Meharg, A. A.; Zhao, F. J., Growing rice aerobically markedly decreases arsenic accumulation. Environmental Science & Technology 2008, 42, 5574-5579. 49. Zavala, Y. J.; Duxbury, J. M., Arsenic in rice: I. estimating normal levels of total arsenic in rice grain. 19



466 467 468 469

Environmental Science & Technology 2008, 42, 3856-3860. 50. Campbell, K. M.; Nordstrom, D. K., Arsenic speciation and sorption in natural environments. Reviews in Mineralogy and Geochemistry 2014, 79, 185-216.

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20


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472

Figure captions

473

Figure 1. Content of As in rice grain and husk

474

Figure 2. Distribution of As species in rice plants tissues

475

Figure 3. Content of As in five tissues of rice plants

476

Figure 4. Distribution of As species in rat organ tissues, urine and feces after 28 days of gavage

477 478 479

administration Figure 5.Mass balanceof As species between the amount administered and the amount of As species detected

21



Figure 1. Content of As in rice grain and husk 61x47mm (300 x 300 DPI)


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Figure 2. Distribution of As species in rice plants tissues 80x94mm (300 x 300 DPI)



Figure 3. Content of As in five tissues of rice plants 80x95mm (300 x 300 DPI)


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Figure 4. Distribution of As species in rat organ tissues, urine and feces after 28 days of gavage administration 80x86mm (300 x 300 DPI)



Figure 5. Mass balance of As species between the amount administered and the amount of As species detected 82x85mm (300 x 300 DPI)


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TOC 85x47mm (300 x 300 DPI)


Comparison of Translocation and Transformation from Soil to Rice and

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