Effect of selenium induced seed priming on arsenic accumulation in rice plant and subsequent transmission in human food chain

Ecotoxicology and Environmental Safety 152 (2018) 67–77

Contents lists available at ScienceDirect

Ecotoxicology and Environmental Safety journal homepage: www.elsevier.com/locate/ecoenv

Effect of selenium induced seed priming on arsenic accumulation in rice plant and subsequent transmission in human food chain

T

⁎

Debojyoti Moulicka, , Subhas Chandra Santraa, Dibakar Ghoshb a b

Department of Environmental Science, University of Kalyani, Nadia, West Bengal, India ICAR - Directorate of Weed Research, Jabalpur, Madhya Pradesh, India

A R T I C L E I N F O

A B S T R A C T

Keywords: Arsenic Rice Seed priming technology Selenium Estimated daily intake (EDI) Cancer risk (CR)

The south-east Asian countries are facing a serious threat of arsenic (As) toxicity due to extensive use of As contaminated groundwater for rice cultivation. This experiment was configured to assess the consequences of rice seed priming with selenium (Se) and cultivation in As free and As contaminated soil. The experiment was arranged in a factorial complete randomized design having two factors viz. seed priming and soil As stress with total twenty-five treatment combinations replicated thrice. Seed priming with Se promotes growth, yield under both As free and As stressed conditions. Se supplementation considerably enhanced the tiller numbers, chlorophyll content, plant height, panicle length and test weight of rice by 23.1%, 23.4%, 15.6% and 30.1%, respectively. When cultivated in As spiked soil and compared with control, Se primed plant enhance growth and yield by reducing As translocation from root to aerial parts, expressed as translocation factor (TF). A reduction of TF root to shoot (46.96%), TF root to husk (36.78–38.01%), TF root to grain (39.63%) can be seen among the Se primed plants than unprimed plants both cultivated in similar As stress. Besides these, a noteworthy reduction in estimated daily intake (EDI) and cancer risk (CR) were also noticed with the consumption of cooked rice obtained after cooking of brown rice of Se primed plants than their unprimed counterparts.

1. Introduction Paddy cultivation in Ganga- Meghna- Brahmaputra basin, located across India and Bangladesh gets affected due to arsenic (As) contaminated soil and groundwater. The well-recognized threat associated with paddy cultivation in those areas is the subsequent transmission of As into food chain through consuming As laden rice as cooked rice. The situation gets even more worsened when As enriched rice cooked along with As contaminated water (Santra and Samal, 2013). Agricultural fields including paddy fields are considered as the source for tons of As gets shipped away into the food chain year after year through irrigation the of As rich groundwater and cultivation in As laden soil (Ali, 2003; Neumann et al., 2011). In the environment especially in the agroecosystem, As use to exists mainly as arsenate (AsV) and arsenite (AsIII) in soil and groundwater (use for irrigation). Besides these AsIII and AsV in the soil environment, the presence of organic As species like methylarsonic acid or dimethylarsinic acid in fractional amount have been also reported (Jia et al., 2012, 2013). Kharif (monsoon) and boro (winter), the two main cropping season has been found to be dominated by two different As species i.e. AsV and AsIII, respectively (Moulick et al., 2016a, b). Speaking of a toxicological aspect of As to plants or

⁎

cultivated crops species, it depends upon chemical forms (organic/inorganic), concentration etc. Plants used to take up AsV, AsIII species by employing different means like phosphate transporters, aquaporin channels{NIPs or nodulin26-like intrinsic proteins} respectively (Asher and Reay, 1979; Ma et al., 2008). On the other hand, organic As were absorbed by plants (rice) using aquaporin Lsi1 (Li et al., 2009). After taking entry into the plant's system, AsV executed it's toxicity by replacing phosphate (PO43-) due to having close resemblance with phosphorus, whereas, AsIII sticks with the sulphahydryl group (-SH) of peptides and interfere with its function (Finnegan et al., 2012). In the paddy field, under submerged / waterlogged soil condition with lower soil pH (acidic), AsV gets reduced in to ASIII. Irrespective of the nature of As species (AsV / AsIII) plant species gets exposed, once inside the plant system AsIII species dominates over other As species (Pickering et al., 2000, 2006). When plants exposed to As in lower concentration gets deposited within the nucleus and cause damage and interfere with replication of nucleic acid and further, upon relocating to leaves photosynthetic machinery gets damaged with pronounced reduction in chlorophyll content by interrupting chlorophyll biosynthesis (Moulick et al., 2017; Mishra et al., 2016, 2014, 2013; Xu et al., 2007; Bhattacharya et al., 2013). Moreover, injurious consequences of As on

Corresponding author. E-mail addresses: [email protected] (D. Moulick), [email protected] (S.C. Santra), [email protected] (D. Ghosh).

https://doi.org/10.1016/j.ecoenv.2018.01.037 Received 29 October 2017; Received in revised form 13 January 2018; Accepted 17 January 2018 0147-6513/ © 2018 Elsevier Inc. All rights reserved.

Ecotoxicology and Environmental Safety 152 (2018) 67–77

D. Moulick et al.

uptake pattern in mature rice plant, grown under As contaminated/ spiked soil either from invivo (field study) or from invitro (controlled study in the pot) investigations. We carried out this experiment with the intention to further enrich our understanding of: (a) influence of Se seed priming on As accumulation pattern by different plant parts on rice; (b) effect of seed priming technology with Se on growth and yield of rice crop and (c) estimate the positive impact of Se seed priming on human health risk associated by consuming rice, grown in As contaminated soil.

rice plant like inhibition of germination and seedling growth (Moulick et al., 2016a), reduces tiller number, biomass and yield of rice (Abedin et al., 2002). Which ultimately leads to higher accumulation of As in rice grain and finally in cooked rice (Moulick et al., 2016a, b; Santra and Samal, 2013; Bhattacharya et al., 2013). The As content in rice grain is mainly governed by the ability of rice plant's (variety) to accumulate As into their root zone and subsequent transfer or translocate of As to grain trough plant system (Bhattacharya et al., 2010). Several attempts have been evaluated as the possible method to restrict the entry of As into grain and subsequently into cooked rice portion. Among the studied methods, organic matter amendment (Rahaman et al., 2011), water management in SRI (systemic rice intensification) - cultivation practice (Thakur et al., 2014), application of phosphorus (as phosphate) and farmyard manure (Mukhopadhyay and Sanyal, 2002), co-application of organic matter and zinc (Zn) in varying amounts to soils (Das et al., 2008), aerobic cultivation (Xu et al., 2008), intermittent ponding (Stroud et al., 2011), water deficit irrigation practice (Mukherjee et al., 2017) etc. were evaluated to reduce As load in rice grain. Beside these practices, developing new rice variety with lower As uptake or translocation potentials (Norton et al., 2009) were also reported. Seed priming is the stimulation of a particular physiological state in plant system by treating with natural and/or synthetic compounds to the seeds before sowing (Jisha et al., 2013) and it has also been proved to be an effective method in imparting stress tolerance to plants. During last few years, several authors reported about the positive outcomes of seed priming as a promising strategy in biotic and abiotic stress management without imposing any genetic/ transgenic alteration. The positive role of selenium (Se) from human and animal as an essential trace mineral is well recognized (Zeng, 2002). Two leading organizations like United States Department of Agriculture and Agency for Toxic Substances and Disease Registry (ASTDR) have set a benchmark value of 55 μg day−1 and ≥ 900 μg day−1 as recommend dietary allowances and toxic levels respectively, for Se (Levander, 1991; ASTDR, 2003; Jukes, 1983). Though the role of Se for plant species is still under consideration but current reports suggest that optimal supplementation of Se (in early stage) is beneficial for plants through improvement of photosynthesis and antioxidative responses. Reactive oxygen species or ROS (generates in the chloroplast or in mitochondria) forms even if plants are cultivated under optimal or normal conditions (both invitro and invivo conditions). According to the opinions of Zhang et al. (2014), Jiang et al. (2015) and Kaur and Nayyar (2015) supplementation of Se improves productivity in common buckwheat (Fagopyrum esculentum moench), mungbean (Vigna radiata L. Wilczek) and in rice (Oryza sativa, L.) respectively. Furthermore, authors like Pilon-Smits and LeDuc (2009) and White and Broadley (2009) found that supplementation with Se significantly improves growth irrespective of the presence of any stressor (i.e. under stressed or absence of stress). Reports also suggest that supplementation of Se can alleviate (when applied in low doses) drought and salinity induced stress mainly diminishing ROS through modulating various enzymatic and nonenzymatic antioxidative machinery (s) in rape seed seedlings (Brassica napus) (Hasanuzzaman et al., 2011; Hasanuzzaman and Fujita, 2011); wheat (Nawaz et al., 2013, 2015); tomato (Solanum lypersicon) (Diao et al., 2014); maize (Zea mays L.) (Jiang et al., 2017) besides these, minimize extreme temperature induced damages in spring wheat (Iqbal et al., 2015); sorghum (Sorghum bicolor L.) plants (Abbas, 2012, 2013) also found. On the other hand, evidence reveals about the ability of Se to execute antagonism against metalloids and metals like As, antimony and other heavy metals have been recognized (Feng et al., 2013; Cao et al., 2013; Zhao et al., 2013; Han et al., 2015). Recently, Moulick et al. (2016a), (2017) reported about positive consequences of priming rice seeds with Se in promoting germination and seedling growth under both ASIII and AsV stress condition in in-vitro condition in non-soil and soil based assay. So far there is no such evidence available that describe the impact of rice seed priming with Se on growth and yield, and As

2. Materials and methods 2.1. Seed priming treatment For this particular experiment high yielding rice variety IET-4094, popularly known as Khitis (with medium and slender grain morphology) was obtained from Regional rice Research Station Chinsurah, West Bengal, India to ensure the absence of any previous history of As contamination. Surface sterilization (with 0.1% HgCl2 solution for 2 min) and seed priming treatments were carried out using sodium selenite solution (Anhydrous Na2SeO3 salt, purchased from HIMEDIA; molecular weight 172.94, ≥ 99% purity) of five different strength (0.0, 0.5, 0.75, 1.0 and 1.25 mg Se L−1) for 24 h in absence of light according to the protocol of Moulick et al. (2016a, b).

2.1.1. Seed bed preparation For preparing seed bed large PVC trays (28 cm length × 20 cm width × 20 cm deep) were used and filled up with garden soil. Before sowing of rice seed, nitrogen, phosphorus and potassium were applied in 1:1:1 ratio (on dry weight basis) in all the trays and irrigated with tap water (Se content < 0.001 mg/L and As content < 0.0003 mg/L). The seed beds were maintained 10 days after transplanting in order to replace damaged seedlings within seven days of transplanting (though no such replacement required).

2.1.2. Pot preparation and experimental layout Bottom sealed earthen pots (40 cm diameter × 40 cm depth) were selected for this experiment. Soil (adjacent to Department of Environmental Science greenhouse, University of Kalyani, having As & Se concentration < 0.0003 mg Kg−1 and < 0.001 mg Kg−1 respectively) from the depth of 15 cm were taken, then the large aggregates were broken by wooden hammer and passed through 2.0 mm stainless steel sieve to obtain a homogeneous mass. For each earthen pot, 5.0 kg soil was poured two days before of transplanting. The available metal (As, Se) content in soil and irrigation water were also analyzed as per methodology of Moulick et al. (2017); whereas, soil physiochemical and textural properties were determined according to the methodology described by Trivedy and Goel (1986) and Kettler et al. (2001), respectively (given in Table 1). A day before transplanting, the pots were spiked with As of different levels (0.0, 10.0, 15.0, 20.0 and 25.0 mg As Kg−1 soil) as a solution of sodium arsenate (sodium arsenate salt; MW312.01, obtained from MERCK, Germany) and pots were kept under with cover. For irrigation purpose tap water (As & Se concentration < 0.0003 mg/L and < 0.001 mg/L respectively) used to ensure As and Se exposure to rice plant only from arsenic spiked soil and Se primed seedlings only (except for unprimed seedlings). Irrigation was carried in such a way that ensure 3–4 cm constant standing water throughout, but irrigation stops ten days before harvesting. The entire experiment was arranged according to factorial complete randomized design (fCRD) having two factors (i) seed priming with Se (five different doses) and (ii) soil As stress (five different As dose) with total twentyfive treatment combinations replicated thrice in seventy five earthen pots. 68

Ecotoxicology and Environmental Safety 152 (2018) 67–77

D. Moulick et al.

day old seedlings can be seen in table S1, table S2.

Table 1 Effects of seed priming and As stress on total arsenic (tAs) content in different plant parts of harvested rice plant as well as in cooked rice. Seed priming

As stress (mg/kg)

Root Unprimed

0.0 10.0 15.0 20.0 25.0 0.50 mg Se/L 0.0 10.0 15.0 20.0 25.0 0.75 mg Se/L 0.0 10.0 15.0 20.0 25.0 1.0 mg Se/L 0.0 10.0 15.0 20.0 25.0 1.25 mg Se/L 0.0 10.0 15.0 20.0 25.0 Sources of Variations As Stress Se seed priming Se × As

2.4. Bio-concentration factor and translocation factor

tAs content (mg/kg)

(1)

Shoot

0.0l 0.0i 6.35k 1.42d-f 10.16i 1.66b-f 14.29f 2.18ab 18.23cd 2.54a 0.0l 0.0i 6.87jk 1.02h 11.08hi 1.16fgh 14.99ef 1.58c-f 18.95bc 2.03abc 0.0l 0.0i 7.36j 0.992h 11.88gh 1.44e-h 15.80e 1.24e-h 19.58b 1.73b-e 0.0l 0.0i 7.66j 0.92h 12.88g 1.00h 17.18d 1.04h 21.49a 1.59c-f 0.0l 0.0i 7.03jk 1.12gh 10.51i 1.11gh 14.62f 1.41e-h 18.83bc 1.95bcd ANOVA F-Values 5694***a 290*** 62.7*** 31.7*** 6.33** 3.95**

Husk

Grain

Cooked rice

0.0j 0.551e-g 0.574b-g 0.652a-d 0.760a 0.0j 0.495f-i 0.524e-i 0.612b-f 0.678abc 0.0j 0.457ghi 0.438hi 0.551d-g 0.623b-e 0.0j 0.425i 0.466ghi 0.495f-i 0.567c-g 0.0j 0.462ghi 0.506e-i 0.52e-i 0.690ab

0.0g 0.130ef 0.183e 0.383bc 0.486a 0.0g 0.100f 0.146ef 0.350cd 0.445ab 0.0g 0.101f 0.152ef 0.341cd 0.424ab 0.0g 0.094f 0.107f 0.301d 0.399bc 0.0g 0.108 f 0.156ef 0.338cd 0.449ab

0.0g 0.069fg 0.095def 0.197abc 0.262a 0.0g 0.062fg 0.091def 0.192abc 0.249ab 0.0g 0.058fg 0.089def 0.156cde 0.208abc 0.0g 0.053fg 0.073efg 0.126c-f 0.195abc 0.0g 0.065fg 0.087def 0.167cd 0.181abc

714*** 22.0*** 2.37*

932*** 11.5*** 1.22 ns

160*** 4.39** 1.18

The bio-concentration factor (BCF) of As were calculated as the ratio of total As content in root to soil; and the translocation factor (TF) of As from root to shoot and onward aerial part including cooked rice were measured as ratio of total As content in that particular part with total As content in root (Rauf et al., 2011). 2.5. Assumption of health risk associated with consumption of cooked rice To assume health risk related to consumption of rice grown in As affected areas; the adult males and females were considered, and they were further divided into sedentary and moderate workers (NNMB, 2002). Here we would like to disclose (as a part of ethical consideration) that during assumption of health risk related to consumption of As laden cooked rice, neither the subjects were injected, ingested with any form of chemical or biochemical forms of As. Moreover, neither blood, urine nor even hair, nail (any kind of biological samples) were collected. The health risk assumption was purely based on the data available (NNMB, 2002). The As burden in cooked rice sample (n = 3) was expressed in terms of total As (tAs). To further elaborate the potential health risk related to As, estimated daily intake (EDI) of As was calculated with minor modification beside the cancer risk (CR), and expressed in the order of 10−4 (Bhatti et al., 2013; Moulick et al., 2016b).

EDI = (C × Fi × Ef × Ed)/(W × Te)

(1)

Cancer Risk (CR) = EDI × CSF

(2)

Here C = total As content (mg Kg−1) in cooked rice, Fi = food intake (cooked rice consumption) by subject (g/person/day) (NNMB, 2002), Ef = exposure frequency (days/year), Ed = exposure duration or life expectancy values of 63.13 years for male and 68.93 years for females of India (United Nations World Population Prospects or UNWPR, 2015), W = average body weight of subject (60 kg for adult i.e. > 18 years old) and Te = average exposure time (Ed × 365 days). CSF stands for cancer slope factor for As (1.5 mg/kg/day).

(1) Values refer to the mean followed by the same letter in a column were not significantly different at P < .05. a F-values. ns: not significant F ratio *, ** and ** indicate significant at P < .05, 0.01 and 0.001, respectively.

2.2. Chlorophyll estimation, harvesting and rice cooking During flowering stage (when panicle initiation started from ˃ 50% of tillers/pot) an active tiller was taken off (2.0 cm above the ground) and chlorophyll was measured from flag leaf following the methods of Anron (1949). Plants were harvested at 125 days after transplanting (DAT) and the panicle length, filled grain, chaff numbers were noted down. Rough rice samples were then dehulled using Satake laboratory sheller. The husk and brown rice were separated, and the brown rice was kept at room temperature before digestion. The non-parboiled brown rice samples were rinsed and cooked with double distilled water in 1:5 ratios (Moulick et al., 2016a, b).

2.6. Statistical analysis Statistical analysis system (SAS for Windows version 9.4) software was used for statistical analysis. The difference among the various treatment combinations was separated using mean value (n = 3) and by applying two way ANOVA using the general linear model procedure (GLM). Further treatment means were separated with the use of Tukey's Honest Significant Difference (HSD) test at a 5% level of significance. 3. Results

2.3. Acid digestion for total As content in different plant parts and quality control

3.1. Arsenic content in different plant parts and cooked rice Before starting acid digestion all the apparatuses were dipped overnight in chromic acid solution and rinsed with double distilled water and dried. Different plant parts including brown rice and cooked rice were digested in block digestion method using 5 mL triacid mixture comprising of 70% perchloric acid, nitric acid and sulphuric acid (all ACS grade) along with SRM (standard reference material, Item no. 1568 A rice flour, and Item no.2709 - San Joaquin Soil both purchased from NIST, USA), beside reagent blanks in triplicate (Moulick et al., 2016a). Total As content was analyzed adopting the external calibration using FI-HG-AAS, Perkin Elmer AAnalyst 400 (flow injection hydride generation atomic absorption spectrometer) with 0.5% NaBH4 dissolved 0.05% NaOH and 10% (v/v) solution of HCl (Koreňovská, 2006). The details of instrumental setup and recovery of As and Se from the respective SRMs and Se content (after priming) in root and shoot of 21-

The As content in different parts of mature rice plant was analyzed and a common trend was observed in both Se primed plants and unprimed. The maximum As accumulation was noticed in rice roots, whereas, the minimal one was found in rice grain (Table 1; Fig. 1(a)). The above trend was further interpreted in terms of bio concentration factor (BCF) and translocation factors. The BCFs and TFs lie in the order of TF root to grain < TF root to husk < TF root to shoot < BCF soil to root (Table 2). It is clear from the result that, the utmost As translocation was observed from root to shoot and the least one from root to the grain of rice. Results suggest that the As accumulation pattern in roots of Se primed plants was 17.57% higher (with higher BCF root/soil) than that of unprimed treatment. But, TF root to shoot, TF root to husk and TF root to grain was 47.0%, 37.4% and 39.6%, respectively lower in Se primed plants as 69

Ecotoxicology and Environmental Safety 152 (2018) 67–77

D. Moulick et al.

Fig. 1. Direct effects of seed priming with Se and As stress on total arsenic (tAs) content and tillers number in rice. Each horizontal bars represents mean (n = 3) value. Columns bearing same letter case (effects of Se- lower case; As stress- upper case)were not significantly different at P < .05.

seed priming. The amount of As (expressed as tAs) ingestion expressed as EDI, increases in a linear fashion with increasing rate of As contamination. On the other hand, as compared to without priming, seed priming with Se markedly reduced the EDI and cancer risk of the human population (irrespective of sex & work pattern), consuming rice grown under As affected areas.

compared to without priming. This phenomenon suggests that Se ameliorate As induced toxicity by confining maximum As content to the root zone and by restricting it's translocation farther into the aerial parts of plants (Tables 1, 2; Fig. 1(a & b)). As compared to without priming, the seed priming with Se diminished the As content in rice grain by 16.92–27.69, 14.75–41.53, 8.61–21.41 and 7.61–17.90% in 10, 15, 20 and 25 mg As Kg−1 stress regime, respectively. Moreover, among the different doses of Se for priming, 1.0 mg Se L−1 was most effective in incarcerating higher amount As in root than the other doses and it also reduced the translocation of As to the aerial parts (Tables 1, 2; Fig. 1(a & b)).

3.2. Effect of seed priming and As stress on plant growth and yield The presence of As in soil markedly reduced the tiller numbers, chlorophyll content, flag leaf area, plant height, panicle length, grain number and test weight (1000 grain weight) of rice by 66.6%, 57.2%, 46.9%, 33%, 46.3%, 44.4% and 52.6%, respectively (Tables 4, 5; Figs. 1(c), 2(a -f)). Whereas, As induced stress prolonged the growth period of rice crop, as a result, the days of flowering was delayed as compared to that of control situation (Table 4 & Fig. 2(c)). On the other hand, Se supplementation through seed priming technology considerably enhanced the tiller numbers, chlorophyll content, flag leaf area, plant height, panicle length, grain number and test weight of rice by 23.1%, 23.4%, 24.6%, 15.6%, 19.0% and 30.1%, respectively. As compared to unprimed treatment, the seed priming with Se was expedited the flowering initiation of the rice plant and reduced the number of chaffy grains per panicle. Significant interactive effect between Se and As was seed on all the growth parameters of rice plant excepting grain numbers (Tables 4, 5).

3.1.1. As content in cooked rice and assumption of EDI and CR Due to the cooking of brown rice with double distilled water, an overall 47.4% reduction in As content has been observed in cooked rice than that of brown rice. As compared to without priming, Se supplementation through seed priming technology with 0.50, 0.75, 1.00 and 1.25 mg Se L−1 effectively reduced the As content in cooked rice by 38.8%, 41.0%, 51.4% and 52.0%, respectively (Table 1; Fig. 1(a)). Findings regarding EDI and CR value presented in Table 3 suggest that adult females were more susceptible to cancer risk compared to the male counterpart (irrespective of workload), due to having higher life expectancy value. The present study also indicates towards the fact that, a considerable amount of As intake might take place if adult population consume rice grain, grown under As affected soil without Se 70

Ecotoxicology and Environmental Safety 152 (2018) 67–77

D. Moulick et al.

Table 2 Effects of seed priming and As stress on bio-concentration factor (BCF) for As in root from soil and translocation factor (TF) from root to shoot, husk, grain and cooked rice. Treatment

BCF (root/soil)

TF

Unprimed seed + 10 mg As/kg Unprimed seed + 15 mg As/kg Unprimed seed + 20 mg As/kg Unprimed seed + 25 mg As/kg Se primed (0.50 mg/L) + 10 mg Se primed (0.50 mg/L) + 15 mg Se primed (0.50 mg/L) + 20 mg Se primed (0.50 mg/L) + 25 mg Se primed (0.75 mg/L) + 10 mg Se primed (0.75 mg/L) + 15 mg Se primed (0.75 mg/L) + 20 mg Se primed (0.75 mg/L) + 25 mg Se primed (1.00 mg/L) + 10 mg Se primed (1.00 mg/L) + 15 mg Se primed (1.00 mg/L) + 20 mg Se primed (1.00 mg/L) + 25 mg Se primed (1.25 mg/L) + 10 mg Se primed (1.25 mg/L) + 15 mg Se primed (1.25 mg/L) + 20 mg Se primed (1.25 mg/L) + 25 mg Sources of Variation As Stress Se seed priming Se × As

(1)

0.222a 0.164b 0.153bc 0.139bcd 0.148bc 0.105c-f 0.106c-f 0.107c-f 0.135bcd 0.120b-e 0.079ef 0.088def 0.120b-e 0.078ef 0.061f 0.074ef 0.159b 0.105c-f 0.097def 0.104c-f

0.0871a 0.0564cde 0.0456e-h 0.0417f-i 0.0723b 0.0473efg 0.0408ghi 0.0358g-j 0.0620bcd 0.0369g-j 0.0349g-j 0.0318hij 0.0556c-f 0.0362g-j 0.0288ij 0.0263j 0.0657bc 0.0481d-g 0.0356g-j 0.0367g-j

0.0203a-d 0.0180b-e 0.0269a 0.0266a 0.0144def 0.0132ef 0.0234ab 0.0235ab 0.0137def 0.0128ef 0.0216abc 0.0216abc 0.0123ef 0.0083f 0.0175b-e 0.0185b-e 0.0153cde 0.0148c-f 0.0232ab 0.0239ab

0.0109a-d 0.0094a-d 0.0138ab 0.0144a 0.0089a-d 0.0082a-d 0.0128abc 0.0131abc 0.0079a-d 0.0075a-d 0.0099a-d 0.0106a-d 0.0068cd 0.0056d 0.0073bcd 0.0091a-d 0.0092a-d 0.0083a-d 0.0115a-d 0.0097a-d

62.7*** 2.93* 8.91***

73.0*** 3.68* 38.3***

14.8*** 2.52 ns 22.5***

5.86** 1.88 ns 3.36**

As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg

0.635e 0.678de 0.715bcd 0.729bcd 0.687bde 0.739bcd 0.750bcd 0.758bc 0.736bcd 0.792ab 0.790ab 0.783ab 0.766bc 0.859a 0.859a 0.860a 0.703cde 0.701cde 0.731bcd 0.753bcd ANOVA F-Values 57.4*** 6.57*** 10.1***

r-s

(root to shoot)

TF

r-h

(root to husk)

TF

r-g

(root to grain)

TF

r-cr

(root to cooked rice)

(1) a

Values refer to the mean followed by the same letter in a column were not significantly different at P < .05. F-values. ns: not significant F ratio *, ** and ** indicate significant at P < .05, 0.01 and 0.001, respectively.

the roots. These can be considered as the possible mechanism (s) behind the execution of antagonism (significant at p < .01 level) by restricting As to root zone and then to shoot (significant at p < .01 level) and husk (significant at p < .05 level) in order to minimize As content in grain and then finally upon cooking in cooked rice too (Table 1 & Table 2; Fig. 1(a)). Rice consumption has been recognized as a potential source of As exposure among the human population; Moulick et al. (2016a, b); Halder et al. (2014) and Davis et al., 2012 supports our current findings. CODEX or the Codex Alimentarious Commission's Committee on Contaminants set up .2 mg kg–1 inorganic As, as the maximum level of As in white (polished) rice. In the present study when the grain As contents were compared with CODEX (Joint FAO/WHO, 2014) recommended value of maximum As content in grain; findings of present investigation suggests that, though majority of the grain As content (irrespective of seed priming treatments) do not fall within the range, but it is noteworthy that CODEX (FAO/WHO, 2014) set the benchmark value for As content in rice grain was based on the As content in white or polished rice. Here in the current study the rice was just dehulled (brown rice) using tabletop rice huller. Findings of Naito et al. (2015) suggests that polishing (with DP95-DP90% or degree of polishing) brown rice (a popular practice) can effectively reduce 61–66% As content, due to effectively removal of bran (during polishing) which usually contain 3–10 fold higher As than the brown rice (Meharg, 2008). So there are ample of opportunity to get it polished (brown rice obtained from Se primed plant cultivated in As spiked soil), rinsed prior to cooking these steps were efficient enough to reduce the As burden from the rice further. The reduction in As content in cooked rice (irrespective priming) upon cooking may ascribed to the fact that upon cooking with double distilled water, water-soluble As (fraction) of brown rice might released into the gruel, discarded later, which supports the findings of Moulick et al. (2016a, b); Bae et al. (2002) (Table 1; Fig. 1(b)). Findings of Karim (2015) suggests regarding MEDI or mean daily intake (from 29 countries) of As were in the range of 1.0 − 0.4 (μg day−1kg−1 BW) for Asian countries and 0.06–0.4 (μg day−1kg−1 BW) with the mean of 0.4 μg day−1kg−1 BW, for a person having 60.0 kg body weight. Results from the current investigation suggests that, the EDI value for As among the adult male and female

The addition of Se through seed priming increased the tiller numbers, chlorophyll content and flag leaf area of rice plant by 1.31, 1.30 and 1.14 fold; it also hastened the reproductive phase of rice plant (Fig. 2c). Besides these, plants were grown under As stress having Se supplementation through seed priming produced considerably longer plant and panicle, higher grain number and greater test weight by 16.0%, 12.9%, 20.4% and 11.2%, respectively than that of rice plant produced under As stress without Se seed priming (Fig. 2d-f). 4. Discussion 4.1. As accumulation and translocation in different plant parts The As accumulation pattern among the various parts found in the order grain < husk < shoot < root supports the findings of Abedin et al. (2002) and Bhattacharya et al. (2013). Greater As content in root than in the shoot can be explained that plant's roots usually considered as the initial point, from where As gets accumulated and then translocated into various plant parts subsequently. Moreover, when rice plant get exposed to As stress, As gets trapped in the apoplast region of root which influences As build up in rice plant by consequent release into the cytosol (Chen et al., 2005). On the other hand, greater As content in the root (with significantly greater BCF value) in Se primed plants than the As the content of unprimed plants was noticed. These findings support the view of Kaur et al. (2017). Findings of Zhou et al. (2017) suggests that supplementation with Se (as fertilizer) effectively reduce As load in the shoot, leaves as well as in rice grain. Till date, the essentiality of Se from plant's nutritional prospect is under consideration (Fordyce, 2013). It is evident that pre-accumulated Se upon germination, distributed with the maximum Se in the roots, which supports the earlier views of Moulick et al. (2017); Hu et al. (2014); Zhu et al. (2009). It can be inferred that accumulated Se might have stimulated phytochelatin synthase (PC) and thus enables the Se primed seedlings (later mature plants) to have greater PC content (Feng and Wei, 2012). Thus, the pre-accumulated Se might have facilitates the formation of greater As-PC/ As-Gs complexes, when cultivated in As spiked pot soil (Tuli et al., 2010) or even by stimulating the formation of insoluble As2Se3 or FeAsSe complexes and makes As to restrict within 71

Ecotoxicology and Environmental Safety 152 (2018) 67–77

0.81 1.12 2.33 3.1 0.73 1.08 2.28 2.95 0.69 1.05 1.84 2.46 0.62 0.86 1.49 2.31 0.77 1.03 1.98 2.15 0.99 1.38 2.86 3.80 0.89 1.32 2.79 3.60 0.85 1.28 2.26 3.00 0.76 1.05 1.83 2.83 0.94 1.26 2.42 2.63

0.71 0.99 2.05 2.72 0.64 0.94 2.00 2.59 0.61 0.93 1.62 2.16 0.55 0.76 1.31 2.03 0.67 0.91 1.74 1.89

Results suggest that As stress inhibited shoot branching ability of the tested variety in a dose-dependent manner in unprimed plants (Table 4; Fig. 1(c)). A similar trend can also be seen in terms of reduction in chl-a and chl-b content in flag leaf during flowering among the unprimed plants. These findings are in good agreement with the previous findings of Abedin et al. (2002), Bhattacharya et al. (2013) and Choudhury et al. (2011). As the induced reduction in chlorophyll content might be due to interrupted electron transport processes in thylakoids and resulted in damage to the chloroplast. Findings from our current investigation also suggest that upon exposed to As stress, flowering time gets delayed by as much as 18.5% in unprimed plants cultivated in 25.0 mg As Kg−1stresss (Table 5; Fig. 2(a,b)). Se primed rice plants cultivated irrespective of soil As stress, showed a significant upward trend in plant growth parameters (tiller number, chlorophyll content, flag leaf area and speed up days of flowering) than the control and unprimed plants cultivated in As spiked soil. It can be assumed that, in Se primed plants cultivated alike the control in As free condition might be due to the ROS (reactive oxygen species) quenching capability of Se experienced reduce ROS induced damages, which might speeds up the growth in a highly significant way (p < .001) (Wu et al., 1998). On the other hand, supplementation of Se in the seeds (before sowing through seed priming) creates a considerable Se pool of primed seeds, later being distributed in root and shoots (Table S2). It is evident that Se was being mostly confined to the root and relatively lesser amount being moved up into the shoot. Results of Table 2 indicates that, in spite of being cultivated in As spiked soil, Se primed plants majority of as load in the root itself (with greater BCF value) in a significant way (p < .001) than the unprimed plants, along with lesser As content in shoot (Moulick et al., 2017). It can be assumed that a significant Se × As interaction leads to modulating the flowering traits in a favourable way (Table 4; Figs. 1(c) and 2(a–c)).

As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg As/kg

#MW- moderate work, SW- sedentary work, NPNL- neither pregnant nor even lactating.

0.79 1.09 2.26 3.01 0.71 1.05 2.21 2.86 0.67 1.02 1.79 2.39 0.61 0.84 1.45 2.24 0.74 0.99 1.92 2.08 0.54 0.75 1.55 2.07 0.49 0.72 1.52 1.97 0.46 0.70 1.23 1.64 0.42 0.57 0.99 1.54 0.51 0.68 1.32 1.43 0.53 0.73 1.51 2.01 0.47 0.70 1.47 1.90 0.45 0.68 1.19 1.59 0.40 0.56 0.97 1.49 0.50 0.67 1.28 1.39 Unprimed seed + 10 mg As/kg Unprimed seed + 15 mg As/kg Unprimed seed + 20 mg As/kg Unprimed seed + 25 mg As/kg Se primed (0.50 mg/L) + 10 mg Se primed (0.50 mg/L) + 15 mg Se primed (0.50 mg/L) + 20 mg Se primed (0.50 mg/L) + 25 mg Se primed (0.75 mg/L) + 10 mg Se primed (0.75 mg/L) + 15 mg Se primed (0.75 mg/L) + 20 mg Se primed (0.75 mg/L) + 25 mg Se primed (1.00 mg/L) + 10 mg Se primed (1.00 mg/L) + 15 mg Se primed (1.00 mg/L) + 20 mg Se primed (1.00 mg/L) + 25 mg Se primed (1.25 mg/L) + 10 mg Se primed (1.25 mg/L) + 15 mg Se primed (1.25 mg/L) + 20 mg Se primed (1.25 mg/L) + 25 mg

0.66 0.92 1.90 2.53 0.59 0.88 1.86 2.40 0.56 0.86 1.50 2.00 0.51 0.70 1.22 1.88 0.63 0.84 1.62 1.75

0.48 0.66 1.37 1.82 0.43 0.63 1.33 1.72 0.40 0.62 1.08 1.44 0.37 0.50 0.88 1.35 0.45 0.60 1.16 1.26

CR-MALE (SW) EDI-FEMALE (NPNL-MW) EDI-FEMALE (NPNL-SW) EDI- MALE (SW)

EDI-MALE (MW)

having 60 kg body weight were higher than the MEDI value for As (Table 3). Above all, when EDI value for As among adult male and female compared to its corresponding WHO recommended PTDI value for As (2.1 μg day−1kg−1 BW), suggests that rice consumption (after cooking) of Se primed plant cultivated in As spiked soil were more effective than that of unprimed plant to minimize few fold of PTWI and associated cancer risk (Table 3). 4.2. Flowering traits of rice plant

Treatment

Table 3 Effects of seed priming and As stress on assumption of estimated daily intake (EDI) of As and cancer risk (CR) associated with consumption of non parboiled rice.

CR-MALE (MW)

CR-FEMALE (NPNL-SW)

CR-FEMALE (NPNL-MW)

D. Moulick et al.

4.3. Growth and yield attributes Plant height reduction under As stress in a dose-dependent fashion in the unprimed plants supports the view of Abedin et al. (2002) and Malik et al. (2010) which may be attributed to inhibition of carbohydrate metabolism. On the other hand, a significant enhancement in plant height noticed among the Se primed plants than the control, may be due to quenching of reactive oxygen species as well as stimulation of carbohydrate metabolism (Moulick et al., 2017; Malik et al., 2010). The enhancement in plant height increases with Se dose from 0.5 mg Se L−1 to 1.0 mg Se L−1 (highest) and then reduced with a further increment to 1.25 mg Se L−1. It may be due to the narrow margin of Se as antioxidant/ essentiality and prooxidant/ toxicity (Moulick et al., 2016a, b) ((Table 5; Fig. 2(d)). From the agronomical point of view, rice yield can be regarded as the consequences of three different components of “source and sink” system. In the current investigation, the drastic reduction in yield of unprimed plants cultivated in the As spiked soil can be seen. It may attribute to the adverse effects of As on source and sink system. The inhibitory effects of As stress can be seen in terms of shorter panicle, reduced number of filled grain per panicle, test weight. And a greater number of unfilled grains (chaffs) can be correlated with reduced chlorophyll (chl-a, chl-b) content, which altered plant architecture associated with the flow of photoassimilates through modulating various 72

Ecotoxicology and Environmental Safety 152 (2018) 67–77

D. Moulick et al.

Table 4 Effects of seed priming and As stress on tillers number, chlorophyll content, flag leaf area and days of flowering in rice. Seed priming

As stress (mg/Kg)

No. of tillers/pot

Chlorophyll-a (mg/g)

Chlorophyll –b (mg/g)

Flag leaf area (cm2)

Days of flowering

(1)

2.84c 1.59i-m 1.30lmn 1.24mn 1.18n 2.94bc 1.61h-l 1.72g-k 1.51i-n 1.41k-n 3.29ab 1.62h-l 1.96e-h 1.85e-i 1.47j-n 3.44a 2.21de 2.09d-g 1.64h-l 1.36k-n 2.39d 2.11def 1.83f-j 1.35lmn 1.27lmn

1.52b 0.95def 0.906e-h 0.76ijk 0.67k 1.55b 1.14c 0.859f-i 0.860f-i 0.7jk 1.58b 1.02cde 0.841f-i 0.94d-g 0.861f-i 2.15a 1.04cd 1.00de 0.805hij 0.789hij 1.63b 0.954def 0.953def 0.815g-j 0.714jk

60.41d 51.45hi 47.46jk 44.78kl 32.03° 66.67c 54.23fgh 51.63hi 47.4jk 37.37n 70.83b 57.57def 50.1ij 53hi 40.47mn 80.07a 59.57de 53.9gh 56.67efg 43.53lm 63.93c 51.45hi 50.27ij 46.4kl 38.43n

92.67hij 100.0d-g 104.7cde 109.0abc 113.7a 87.00k 94.33hij 99.00f-i 103.7c-f 110.7ab 83.33kl 92.67hij 94.67hij 103.7c-f 108.7abc 79.67l 93.33e-i 93.33hij 99.00f-i 106.0bcd 86.33k 94.33hij 99.00f-i 99.00f-i 108.3abc

439*** 42.1*** 12.1***

1419*** 54.5*** 32.5***

1544*** 253.7*** 14.9***

395*** 63.4*** 2.54*

30.0c 21.33de 17.66h 14.66jk 10.0l 34.66b 25.33c 20.33def 16.66hi 16.00hi 36.33ab 23.33efg 21.33de 17.33h 18.66g 37.33a 25.66c 21.66de 16.33hi 19.66fg 30.66c 21.00de 20.33f 15.33j 19.66fg ANOVA F-values 332***a 29.1*** 3.68**

Unprimed

0.0 10.0 15.0 20.0 25.0 0.50 mg Se/L 0.0 10.0 15.0 20.0 25.0 0.75 mg Se/L 0.0 10.0 15.0 20.0 25.0 1.0 mg Se/L 0.0 10.0 15.0 20.0 25.0 1.25 mg Se/L 0.0 10.0 15.0 20.0 25.0 Sources of Variations As Stress Se seed priming Se × As

(1) a

Values refer to the mean followed by the same letter in a column were not significantly different at P < .05. F-values. F ratio *, ** and ** indicate significant at P < .05, 0.01 and 0.001, respectively.

Table 5 Effects of seed priming and As stress on plant height, panicle length, grain number and test weight of rice. Seed priming Unprimed

As stress (mg/Kg)

0.00 10.0 15.0 20.0 25.0 0.50 mg Se/L 0.0 10.0 15.0 20.0 25.0 0.75 mg Se/L 0.0 10.0 15.0 20.0 25.0 1.0 mg Se/L 0.0 10.0 15.0 20.0 25.0 1.25 mg Se/L 0.0 10.0 15.0 20.0 25.0 Sources of Variations As Stress Se seed priming Se × As

Plant height (cm) (1)

cd

121.4 92.8h-k 88.3ijk 80.6k 81.0k 126.1bc 106.8efg 97.3f-i 92.7h-k 83.3jk 135.1ab 108.2def 98.5f-i 95.9f-j 104.5f-h 143.8a 119.7cde 91.6h-k 91.1h-k 96.4f-j 123.9bc 93.7g-k 92.5h-k 91.9h-k 89.6ijk ANOVA F-values 222***a 33.6*** 4.37***

Panicle length (cm) bc

No. of grains/pot c

34.3 28.2ef 24.8h 20.2jk 18.4k 35.5b 30.5de 25.6gh 21.8ij 20.0jk 40.5 a 31.4d 27.7fg 24.2hi 24.6h 42.5a 32.8cd 26.3fgh 20.1jk 21.2j 34.5bc 30.8d 28.3ef 22.1ij 20.6jk

1018 1041ab 952cd 783ef 714g 1228 1051ab 957cd 837de 814e 1224a 1085ab 954cd 877d 760ef 1285a 1127b 1031ab 876d 798f 1151b 1025cd 966c 794f 713g

1216*** 76.9*** 15.8***

2.59* 1.23 ns 0.11 ns

(1) a

No. of chaffy grains/pot e

73

c

136 153c 164ab 172a 168a 113h 117hij 152c 172a 168a 106ijk 116hij 143d 159bc 127ef 90k 96jk 144d 153bc 111hi 109hij 109hij 156bc 153bc 125efg

Values refer to the mean followed by the same letter in a column were not significantly different at P < .05. F-values. ns: not significant F ratio *, ** and ** indicate significant at P < .05, 0.01 and 0.001, respectively.

No. of filled grains/pot

45.9*** 22.5*** 2.00*

Test weight (g)

982 888c-f 788i 611l 546lm 1115bc 934c-e 805h 665k 646i-l 1118b 969cd 811hi 718j 633kl 1195a 1031ab 887g 723ij 687jk 1042ab 916cde 810hi 641k 588kl

16.67d 12.00fg 8.70hi 8.23i 7.97i 19.40bc 12.57efg 9.40hi 8.37i 8.23i 21.30b 13.20ef 9.17hi 8.73hi 8.20i 24.13a 14.37e 10.60gh 9.60hi 8.90hi 19.27c 12.30gf 9.07hi 8.30i 8.03i

364*** 27.4*** 1.04 ns

916*** 40.9*** 7.38***

Ecotoxicology and Environmental Safety 152 (2018) 67–77

D. Moulick et al.

Fig. 2. Direct effects of seed priming with Se and As stress on chlorophyll content (a), flag leaf area (b) and days of flowering (c) in rice. Each horizontal bars represents mean (n = 3) value. Columns bearing same letter case (effects of Se- lower case; As stress- upper case)were not significantly different at P < .05.

with higher grain and greater test weight. The restoration of as induced inhibition on selected yield attributes due to the execution of antagonism between Se and As and to restrict the upward movement of As from root (Section 4.1). With comparatively lesser As content into the shoot (significantly lesser than unprimed plants also) leads to modulate chlorophyll content, reduced days of flowering and most importantly flag leaf area which intern enhanced yield (Kaur et al., 2017) (Table 5;Fig. 2(e,f)). In case of Se primed plants cultivated in As free soil alike the control, also posses significantly (p < .001) greater test weight, grain number, filled grain beside lesser chaff than the control may attribute to larger flag leaf area (Khush, 2013) suggests the positive role of Se in enhancing rice yield (Tables 4, 5).(Fig. 3)

transporters (Xing and Zhang, 2010) (Table 5; Fig. 2(a)). Nakagawa et al. (2002) found that, the number of grains per panicle governed by the spikelets numbers and it's seed setting rates, which in turn further influenced by a number of factors such as the size of the panicle (panicle length here). The As induced reduction in tiller number, reduction in flag leaf area, chlorophyll content and panicle length can be attributed behind the reduction in grain number per panicle (p < .05). Further, if flowering gets delayed in stressful environmental condition, grain filling may be compromised i.e. the number of chaffs gets increased (Norton et al., 2013; Gao et al., 2014) supports the findings of the current investigation (Table 5; Fig. 2(e)). In this particular experiment with increase in As stress from 10. to 25.0 mg As Kg−1 the chaff number increased in a significant way (at p < .001 level) from 153 to 168 against 136 in control, which may be attributed to the As induced injuries due to oxidative stress in dose-dependent fashion (Section 4.1). Finally, rice grain formation during grain filling phase is an outcome of cell division takes place both latitudinally as well as longitudinally modulated by ubiquitin-proteasome and cell-wall invertases (Xing and Zhang, 2010). Noteworthy reduction of test weight in a dose/stress (As stress in pot soil here) dependent manner among the unprimed plants might be due to the As induced negative or down-regulation of ubiquitin-proteasome and cell-wall invertase, yet to be confirmed. Under similar As stress regimes and compared to the unprimed plants, Se primed plants upon harvesting showed to have longer panicle length

5. Conclusion Prior to this article, there is numerous evidence exist that describe the potential of seed priming in alleviating various stress induced by biotic and abiotic components on various crops. An earlier ameliorating aspect of Se species against As derived from outcomes from hydroponics investigation as well as an investigation carried out in petriplates, during germination and on seedling stage. In order to convey the benefits of Se in promoting growth and execute antagonism against As stress, we supplemented the seeds with Se, before cultivation using seed priming technology in order to merge the gap between laboratory and 74

Ecotoxicology and Environmental Safety 152 (2018) 67–77

D. Moulick et al.

Fig. 3. Direct effects of seed priming with Se and As stress on plant height and panicle length (a), grain numbers (b) and 1000 seed weight or test weight (c) of rice. Each horizontal bars represents mean (n = 3) value. Columns bearing same letter case (effects of Se- lower case; As stress- upper case)were not significantly different at P < .05.

field. The findings suggest that Se primed plants had higher chlorophyll content, tiller number, test weight along with less chaff than the control when cultivated alike the control. The trend of enhanced growth and yield can also be seen, even when cultivated in series of As contaminated soil than their respective unprimed counterparts, by restricting maximum As load into the shoot along with significant reduction in As content grain as well as in brown rice. Findings from this particular study also show, that consumption of brown rice obtained particularly from Se primed plants cultivated in As spiked soil may significantly reduce As exposure to the population than the brown rice of unprimed plants cultivated in similar As stress. If further investigation carried out in large-scale, seed priming with selenium could emerge out to be an alternative, cheap and farmerfriendly mitigation option to As induced damage in rice.

Conflict of interest We the authors don’t have any kind of conflict (s). Appendix A. Supplementary material Supplementary data associated with this article can be found in the online version at http://dx.doi.org/10.1016/j.ecoenv.2018.01.037. References Abbas, S.M., 2012. Effects of low temperature and selenium application on growth and the physiological changes in sorghum seedlings. J. Stress Physiol. Biochem. 8, 268–286. Abbas, S.M., 2013. Low levels of selenium application attenuate low temperature stress in sorghum (Sorghum bicolor L.) seedlings. Pak. J. Bot. 45, 1597–1604. Abedin, M.J., Cotter-Howells, J., Meharg, A.A., 2002. Arsenic uptake and accumulation in rice (Oryza sativa L.) irrigated with contaminated water. Plant Soil. 240 (2), 311–319. Ali, M.A., 2003. Ate of arsenic in the environment. In: Ahmed, M.F. (Ed.), Arsenic Contamination: Bangladesh Perspective. ITN-Bangladesh, Dhaka, Bangladesh, pp. 84–100. Arnon, D.I., 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24 (1), 1. ATSDR, 2003. Toxicological Profile for Selenium. Agency for Toxic Substances and

Acknowledgements The authors are cordially thankful to University of Kalyani for providing Net House and laboratory facility and Ministry of Environment and Forest, Government of West Bengal, India for providing fellowship. 75

Ecotoxicology and Environmental Safety 152 (2018) 67–77

D. Moulick et al.

radiata L. Wilczek) plants reduces sodium uptake, improves reproductive function, pod set and seed yield. Sci. Hortic. 197, 304–317. Kettler, T.A., Doran, J.W., Gilbert, T.L., 2001. Simplified method for soil particle-size determination to accompany soil-quality analyses. Soil Sci. Soc. Am. J. 65, 849–852. Khush, G.S., 2013. Strategies for increasing the yield potential of cereals: case of rice as an example. Plant Breed. 132 (5), 433–436. Koreňovská, M., 2006. Determination of arsenic, antimony, and selenium by FI-HG-AAS in foods consumed in Slovakia. J. Food Nutr. Res. 45 (2), 84–88. Levander, O.A., 1991. Scientific rationale for the 1989 recommended dietary allowance for selenium. J. Am. Diet. Assoc. 91 (12), 1572–1576. Li, R.Y., Ago, Y., Liu, W.J., Mitani, N., Feldmann, J., McGrath, S.P., Ma, J.F., Zhao, F.J., 2009. The rice aquaporin Lsi1 mediates uptake of methylated arsenic species. Plant Physiol. 150, 2071–2080. Ma, J.F., Yamaji, N., Mitani, N., Xu, X.Y., Su, Y.H., McGrath, S.P., Zhao, F.J., 2008. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc. Natl. Acad. Sci. USA 105, 9931–9935. Malik, J.A., Kumar, S., Thakur, P., Sharma, S., Kaur, N., Kaur, R., Pathania, D., Bhandhari, K., Kaushal, N., Singh, K., Srivastava, A., Nayyar, H., 2010. Promotion of growth in Mungbean (Phaseolus aureus Roxb.) by selenium is associated with stimulation of carbohydrate metabolism. Biol. Trace Elem. Res. 143, 530–539. Meherg, A.A., Lombi, E., Williams, P.N., Scheckel, K., Feldmann, J., Raab, A., Zhu, Y.-G., Islam, R., 2008. Speciation and localization of arsenic in white and brown rice grains. Environ. Sci. Technol. 42, 1051–1057. Mishra, S., Alfeld, M., Sobotka, R., Andresen, E., Falkenberg, G., Küpper, H., 2016. Analysis of sub-lethal arsenic toxicity to Ceratophyllum demersum: subcellular distribution of arsenic and inhibition of chlorophyll biosynthesis. J. Exp. Bot. 67, 4639–4646. Mishra, S., Stärk, H.-J., Küpper, H.A., 2014. Different sequence of events than previously reported leads to arsenic-induced damage in Ceratophyllum demersum L. Metallomics 6, 444–454. Mishra, S., Wellenreuther, G., Mattusch, J., Stärk, H.J., Küpper, H., 2013. Speciation and distribution of arsenic in the nonhyperaccumulator macrophyte Ceratophyllum demersum. Plant Physiol. 163, 1396–1408. Moulick, D., Ghosh, D., Santra, S.C., 2016a. An assessment of some physicochemical properties and cooking characteristics of milled rice and associated health risk in two rice varieties of arsenic contaminated areas of West Bengal, India. Int. J. Agric. Food Sci. 6 (2), 44–55. Moulick, D., Ghosh, D., Santra, S.C., 2016b. Evaluation of effectiveness of seed priming with selenium in rice during germination under arsenic stress. Plant Physiol. Biochem. 109, 571–578. Moulick, D., Santra, S.C., Ghosh, D., 2017. Seed priming with Se alleviate As induced phytotoxicity during germination and seedling growth by restricting As translocation in rice (Oryza sativa L c.v. IET-4094). Ecotoxicol. Environ. Saf. 145, 449–456. Mukhopadhyay, D., Sanyal, S.K., 2002. Effect of phosphate, arsenic and farmyard manure on the changes of the extractable arsenic in some soils of West Bengal and reflection thereof on crop uptake. In: Proceedings of the Natl. Seminar on Developments in Soil Science. Indian Soc. Soil Sci., Nagpur, December. 28–31. Mukherjee, A., Kundu, M., Basu, B., Sinha, B., Chatterjee, M., Bairagya, M.D., Singh, U.K., Sarkar, S., 2017. Arsenic load in rice ecosystem and its mitigation through deficit irrigation. J. Environ. Manag. 197, 89–95. Naito, S., Matsumoto, E., Shindoh, K., Nishimura, T., 2015. Effects of polishing, cooking, and storing on total arsenic and arsenic species concentrations in rice cultivated in Japan. Food Chem. 168, 294–301. Nakagawa, M., Shimamoto, K., Kyozuka, J., 2002. Overexpression of RCN1 and RCN2, rice terminal flower 1/CENTRORADIALIS homologs, confers delay of phase transition and altered panicle morphology in rice. Plant J. 29, 743–750. Nawaz, F., Ashraf, M.Y., Ahmad, R., Waraich, E.A., 2013. Selenium (Se) seed priming induced growth and biochemical changes in wheat under water deficit conditions. Biol. Trace Elem. Res. 151, 284–293. Nawaz, F., Ahmad, R., Ashraf, M.Y., Waraich, E.A., Khan, S.Z., 2015. Effect of selenium foliar spray on physiological and biochemical processes and chemical constituents of wheat under drought stress. Ecotoxicol. Environ. Saf. 113, 191–200. Neumann, R.B., St. Vincent, A.P., Roberts, L.C., Badruzzaman, A.B., Ali, M.A., Harvey, C.F., 2011. Rice field geochemistry and hydrology: an explanation for why groundwater irrigated fields in Bangladesh are net sinks of arsenic from groundwater. Environ. Sci. Technol. 45, 2072–2078. NNMB, 2002. Diet and Nutritional Status of Rural Population. Report by National Institute of Nutrition. Indian Council of Medical Research, Hyderabad. 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., 2009. Identification of low inorganic and total grain arsenic rice cultivars from Bangladesh. Environ. Sci. Technol. 43 (15), 6070–6075. Norton, G.J., Adomako, E.E., Deacon, C.M., Carey, A.M., Price, A.H., Meharg, A.A., 2013. Effect of organic matter amendment, arsenic amendment and water management regime on rice grain arsenic species. Environ. Pollut. 177, 38–47. Pickering, I.J., Prince, R.C., George, M.J., Smith, R.D., George, G.N., Salt, D.E., 2000. Reduction and coordination of arsenic in Indian mustard. Plant Physiol. 122, 1171–1177. Pickering, I.J., Gumaelius, L., Harris, H.H., Prince, R.C., Hirsch, G., Banks, J.A., Salt, D.E., George, G.N., 2006. Localizing the biochemical transformations of arsenate in a hyperaccumulating fern. Environ. Sci. Technol. 40, 5010–5014. Pilon-Smits, E.A., LeDuc, D.L., 2009. Phytoremediation of selenium using transgenic plants. Curr. Opin. Biotechnol. 20, 207–212. Rahaman, S., Sinha, A.C., Mukhopadhyay, D., 2011. Effect of water regimes and organic matters on transport of arsenic in summer rice (Oryza sativa L.). J. Environ. Sci. 23 (4), 633–639.

Disease Registry, Atlanta, GA. http://www.atsdr.cdc.gov/ToxProfiles/tp.asp?id = 153&tid = 28. Asher, C.J., Reay, P.F., 1979. Arsenic uptake by barley seedlings. Aust. J. Plant Physiol. 6, 459–466. Bae, M., Watanabe, C., Inaoka, T., Sekiyama, M., Sudo, N., Bokul, M.H., Ohtsuka, R., 2002. Arsenic in cooked rice in Bangladesh. Lancet 360, 1839–1840. Bhattacharya, P., Samal, A.C., Majumdar, J., Banerjee, S., Santra, S.C., 2013. In vitro assessment on the impact of soil arsenic in the eight rice varieties of West Bengal, India. J. Hazard. Mater. 262, 1091–1097. Bhattacharya, P., Samal, A.C., Majumdar, J., Santra, S.C., 2010. Accumulation of arsenic and its distribution in rice plant (Oryza sativa L.) in Gangetic West Bengal. India Paddy Water Environ. 8, 63–70. http://dx.doi.org/10.1007/s10333-009-0180-z. Bhatti, S.M., Anderson, C.W., Stewart, R.B., Robinson, B.H., 2013. Risk assessment of vegetables irrigated with arsenic-contaminated water. Environ. Sci. Process Impacts 15 (10), 1866–1875. Cao, F., Wang, N., Zhang, M., Dai, H., Dawood, M., Zhang, G., Wu, F., 2013. Comparative study of alleviating effects of GSH, Se and Zn under combined contamination of cadmium and chromium in rice (Oryza sativa). Biometals 26, 297–308. Choudhury, B., Chowdhury, S., Biswas, A.K., 2011. Regulation of growth and metabolism in rice (Oryza sativa L.) by As and its possible reversal by phosphate. J. Plant Interact. 6, 15–24. Chen, T., Yan, X., Liao, X., Xiao, X., Huang, Z., Xie, H., Zhai, L., 2005. Subcellular distribution and compartmentalization of As in Pteris vittata L. Chin. Sci. Bull. 50, 2843–2849. Das, D.K., Sur, P., Das, K., 2008. Mobilization of arsenic in soils and in rice (Oryza sativa L.) plant affected by organic matter and zinc application in irrigation water contaminated with arsenic. Plant Soil Environ. 54 (1), 30–37. Diao, M., Ma, L., Wang, J., Cui, J., Fu, A., Liu, H.Y., 2014. Selenium promotes the growth and photosynthesis of tomato seedlings under salt stress by enhancing chloroplast antioxidant defense system. J. Plant Growth Regul. 33 (3), 671–682. Feng, R.W., Wei, C.Y., 2012. Antioxidative mechanisms on selenium accumulation in Pteris vittata L., a potential selenium phytoremediation plant. Plant Soil Environ. 58 (3), 105–110. Feng, R., Wei, C., Tu, S., 2013. The roles of selenium in protecting plants against abiotic stresses. Environ. Exp. Bot. 87, 58–68. Finnegan, P.M., Chen, W., 2012. Arsenic toxicity: the effects on plant metabolism. Front. Physiol. 3, 182. Fordyce, F.M., 2013. Selenium deficiency and toxicity in the environment. In: Selinus, O. (Ed.), Essentials of Medical Geology. Springer, Dordrecht, pp. 375–416. Gao, H., Jin, M., Zheng, X.M., Chen, J., Yuan, D., Xin, Y., Sheng, P., 2014. Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. PNAS 111 (46), 16337–16342. Halder, D., Biswas, A., lejkovec, Z., Chatterjee, D., Nriagu, J., Jacks, G., Bhattacharya, P., 2014. Arsenic species in raw and cooked rice: implications for human health in rural Bengal. Sci. Total Environ. 1.497, 200–208. Han, D., Xiong, S., Tu, S., Liu, J., Chen, C., 2015. Interactive effects of selenium and arsenic on growth, antioxidant system, arsenic and selenium species of Nicotiana tabacum L. Environ. Exp. Bot. 117, 12–19. Hasanuzzaman, M., Hossain, M.A., Fujita, M., 2011. Selenium-induced upregulation of the antioxidant defense and methylglyoxal detoxification system reduces salinityinduced damage in rapeseed seedlings. Biol. Trace Elem. Res. 143, 1704–1721. Hasanuzzaman, M., Fujita, M., 2011. Selenium pretreatment upregulates the antioxidant defense and methylglyoxal detoxification system and confers enhanced tolerance to drought stress in rapeseed seedlings. Biol. Trace Elem. Res. 143, 1758–1776. Hu, Y., Duan, G.L., Huang, Y.Z., Liu, Y.X., Sun, G.X., 2014. Interactive effects of different inorganic As and Se species on their uptake and translocation by rice (Oryza sativa L.) seedlings. Environ. Sci. Pollut. Res. 21, 3955–3962. Iqbal, M., Hussain, I., Liaqat, H., Ashraf, M.A., Rasheed, R., Rehman, A.U., 2015. Exogenously applied selenium reduces oxidative stress and induces heat tolerance in spring wheat. Plant Physiol. Biochem. 94, 95–103. Jia, Y., Huang, H., Sun, G.X., Zhao, F.J., Zhu, Y.G., 2012. Pathways and relative contributions to arsenic volatilization from rice plants and paddy soil. Environ. Sci. Technol. 46, 8090–8096. Jia, Y., Sun, G.X., Huang, H., Zhu, Y.-G., 2013. Biogas slurry application elevated arsenic accumulation in rice plant through increased arsenic release and methylation in paddy soil. Plant Soil 365, 387–396. Jiang, C., Zu, C., Lu, D., Zheng, Q., Shen, J., Wang, H., Li, D., 2017. Effect of exogenous selenium supply on photosynthesis, Na+ accumulation and antioxidative capacity of maize (Zea mays L.) under salinity stress. Sci. Rep. 7, 42039. http://dx.doi.org/10. 1038/srep42039. Jiang, Y., Zeng, Z.H., Bu, Y., Ren, C.Z., Li, J.Z., Han, J.J., Tao, C., Zhang, K., Wang, X.X., Li, Y.J., Lu, G.X., Hu, Y.G., 2015. Effects of selenium fertilizer on grain yield, se uptake and distribution in common buckwheat (Fagopyrum esculentum moench). Plant Soil Environ. 61, 371–377. Jisha, K.C., Vijayakumari, K., Puthur, J.T., 2013. Seed priming for abiotic stress tolerance: an overview. Acta Physiol. Plant. 35, 1381–1396. Joint FAO/WHO Food Standards Programme CODEX Alimentarius Commission, 2014. Report of the Eighth Session of the CODEX Committee on Contaminants in Foods. The Hague, The Netherlands. Jallad, Karim N., 2015. Heavy metal exposure from ingesting rice and its related potential hazardous health risks to humans. Environ. Sci. Pollut. Res. http://dx.doi.org/10. 1007/s11356-015-4753-7. Kaur, S., Singh, D., Singh, K., 2017. Effect of selenium application on arsenic uptake in rice (Oryza sativa L.). Environ. Monit. Assess. http://dx.doi.org/10.1007/s10661017-6138-5. Kaur, S., Nayyar, H., 2015. Selenium fertilization to salt-stressed mungbean (Vigna

76

Ecotoxicology and Environmental Safety 152 (2018) 67–77

D. Moulick et al.

levels upon growth of rice and its accumulation. J. Hunan Agric. Univ. 24, 176–179. Xing, Y., Zhang, Q., 2010. Genetic and molecular bases of rice yield. Annu. Rev. Plant Biol. 61, 421–442. Xu, X.Y., McGrath, S.P., Zhao, F.J., 2007. Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol. 176, 590–599. Xu, X.Y.S., McGrath, P., Meharg, A.A., et al., 2008. Growing rice aerobically markedly decreases arsenic accumulation. Environ. Sci. Technol. 42, 5574–5579. Zeng, H., 2002. Selenite and selenomethionine promote HL-60 cell cycle progression. J. Nutr. 132, 674–679. Zhang, M., Tang, S., Huang, X., Zhang, F., Pang, Y., Huang, Q., 2014. Selenium uptake, dynamic changes in selenium content and its influence on photosynthesis and chlorophyll fluorescence in rice (Oryza sativa, L.). Environ. Exp. Bot. 107, 39–45. Zhao, J., Gao, Y., Li, Y.F., Hu, Y., Peng, X., Dong, Y., Li, B., Chen, C., Chai, Z., 2013. Selenium inhibits the phytotoxicity of mercury in garlic (Allium sativum). Environ. Res. 125, 75–81. Zhu, Y.G., Pilon-Smits, E.A.H., Zhao, F.J., Williams, P.N., Meharg, A.A., 2009. Selenium in higher plants: understanding mechanisms for biofortification and phytoremediation. Trends Plant Sci. 14, 436–442. Zhou, X.B., Gao, A.X., Lai, F., Zhang, C.M., Xu, W.H., 2017. The role of selenium in soil: effect on the uptake and translocation of arsenic in rice (Oryza sativa). Int. J. Agric. Biol. 19 (5), 1227–1234.

Rauf, M.A., Hakim, M.A., Hanafi, M.M., Islam, M.M., Rahman, G.K., Panaullah, G.M., 2011. Bioaccumulation of arsenic (As) and phosphorous by transplanting Aman rice in arsenic-contaminated clay soils. Aust. J. Crop Sci. 1. 5 (12), 1678. Santra, S.C., Samal, A.C., 2013. Arsenic scenario in Gangetic delta of West Bengal: risk and management. Dev. Eco. Scan 8, 41–55. Stroud, J.L., Norton, G.J., Islam, M.R., Dasgupta, T., White, R.P., Price, A.H., Meharg, A.A., McGrath, S.P., Zhao, F.J., 2011. The dynamics of arsenic in four paddy fields in the Bengal delta. Environ. Pollut. 159 (4), 947–953. Thakur, A.K., Mohanty, R.K., Patil, D.U., Kumar, A., 2014. Impact of water management on yield and water productivity with system of rice intensification (SRI) and conventional transplanting system in rice. Paddy Water Environ 12. pp. 413–424. Trivedy, R.K., Goel, P.K., 1986. Chemical and Biological Methods for Water Pollution Studies. Environmental Publication, Karad, Maharashtra, pp. 92–107. Tuli, R., Chakrabarty, D., Trivedi, P.K., Tripathi, R.D., 2010. Recent advances in arsenic accumulation and metabolism in rice. Mol. Breed. 26 (2), 307–323. United Nations World Population Prospects, 2015. 2015 revision" United Nations Department of Economic and Social Affairs (29 July. White, P.J., Broadley, M.R., 2009. Biofortification of crops with seven mineral elements often lacking in human diets – iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol. 182, 49–84. Wu, Y.Y., Luo, Z.M., Peng, Z.K., 1998. Research on influence of Se provided at different

77