Next Article in Journal
NADH-GOGAT Overexpression Does Not Improve Maize (Zea mays L.) Performance Even When Pyramiding with NAD-IDH, GDH and GS
Previous Article in Journal
Investigation of the EIL/EIN3 Transcription Factor Gene Family Members and Their Expression Levels in the Early Stage of Cotton Fiber Development
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 9
Issue 2
10.3390/plants9020129
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Arsenic Uptake and Accumulation Mechanisms in Rice Species

by
Tayebeh Abedi
1,* and
Amin Mojiri
2
1
Umea Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 90183 Umea, Sweden
2
Department of Civil and Environmental Engineering, Graduate School of Civil Engineering, Hiroshima University, 1-4-1 Kagamiyama, Higashihiroshima 739-8527, Japan
*
Author to whom correspondence should be addressed.
Plants 2020, 9(2), 129; https://doi.org/10.3390/plants9020129
Submission received: 27 December 2019 / Revised: 16 January 2020 / Accepted: 20 January 2020 / Published: 21 January 2020
Browse Figure
Versions Notes

Abstract

:
Rice consumption is a source of arsenic (As) exposure, which poses serious health risks. In this study, the accumulation of As in rice was studied. Research shows that As accumulation in rice in Taiwan and Bangladesh is higher than that in other countries. In addition, the critical factors influencing the uptake of As into rice crops are defined. Furthermore, determining the feasibility of using effective ways to reduce the accumulation of As in rice was studied. AsV and AsIII are transported to the root through phosphate transporters and nodulin 26-like intrinsic channels. The silicic acid transporter may have a vital role in the entry of methylated As, dimethylarsinic acid (DMA) and monomethylarsonic acid (MMA), into the root. Amongst As species, DMA(V) is particularly mobile in plants and can easily transfer from root to shoot. The OsPTR7 gene has a key role in moving DMA in the xylem or phloem. Soil properties can affect the uptake of As by plants. An increase in organic matter and in the concentrations of sulphur, iron, and manganese reduces the uptake of As by plants. Amongst the agronomic strategies in diminishing the uptake and accumulation of As in rice, using microalgae and bacteria is the most efficient.

Graphical Abstract

1. Introduction

Rice (Oryza sativa L.) provides food for more than three billion people [1]. Approximately 90% of rice production and consumption is reported in Asia [2]. By 2050, the production of rice should rise by 60%–70% to meet the requirements of the predicted population growth in Asia [3]. Rice can be cultivated in many regions of the world because of its resourcefulness and diversity. Two species, Oryza glaberrima Steud. (in Africa) and Oryza sativa L. (in Asia), are commonly cultivated [4]. However, rice consumption can pose problems because of the arsenic (As) accumulation in rice and thus serves a vital source of As exposure in humans [5].
As is the 20th abundant component on the Earth’s crust. However, As is a toxic metalloid and is remarked as a considerable global groundwater contaminant, affecting certain rivers and deltas in East and South Asia and in South American countries [6]. Based on the Agency for Toxic Substances and Disease Registry list 2017, As is amongst the most hazardous materials that could be poisonous to humans. Approximately 200 million people in around 70 countries have been exposed to this metalloid [7].
As enters agricultural lands and the environment via natural sources, such as rocks, As-enriched minerals, forest fires, volcanoes and anthropogenic sources (e.g., mining, herbicides, phosphate fertilisers, smelting, industrial processes, coal combustion and timber preservatives) [8]. The average amount of As in agricultural fields that receive As-comprising pesticides and defoliants ranges from 5 mg/kg to 2553 mg/kg [9]. The management of paddy soils for the wet cultivation of rice involves different cycles of submerged and dry days, which cause alternating oxidising and reducing processes in soil. Under this condition in paddy soil, As is reduced to arsenite (AsIII) with high toxicity and mobility in flooded soil, AsIII may then be taken up by rice [10]. Evidence shows considerable As toxicity from the utilisation of rice and rice-based products, especially those consumed as a staple dietary source [11]. Accumulation of As in rice may be decreased by amending cultural practices. Hence, the current work focused on the mechanisms of uptake and accumulation of As in rice and the effective factors which reduce As uptake by rice crops. The results are expected to enrich our understanding of the uptake, transport and distribution of As in rice.

2. Arsenic Uptake and Transport by Rice Plants

Rice is more seriously affected by As pollution than other crop plants. Its cultivation is carried out in flooded conditions, which lead to the reduction conditions [12]. As may be found in the environment, organic and inorganic AsIII and arsenate (AsV) are the dominant As species that reduce paddy soil conditions, followed by methylated As species. Moreover, plant roots selectively may uptake specific As forms [13]. Table 1 shows the reported concentrations of As in rice around the world. All As species can be transferred through the plant cell via specific transporter proteins [14]. The genes involved in transporting As in rice are shown in Table 2.

2.1. Uptake of Inorganic Arsenic

Inorganic As, AsIII and AsV, is more toxic than organic As, dimethylarsinic acid (DMA) and monomethylarsonic acid (MMA) [18]. Inorganic As is the dominant form of As in soil and groundwater. Under aerobic conditions in soil, AsV dominates, whereas, in submerged conditions, AsIII is the dominant species [40].
AsV may generally enter the roots of rice crops through phosphate transporters (PHTs), primarily PHT1 (phosphate transporter1)-type transporters [41] during the regulation of inorganic phosphorous (Pi) [42]. A total of 13 PHTs from the PHT1 family in rice (Oryza sativa) have been found to mediate Pi uptake and transport [43] through the highly efficient silicon (Si) uptake pathway.
Furthermore, AsIII may enter by the nodulin 26-like intrinsic (NIPs) aquaporin channels accompanied by silicic acid and ammonia [42]. NIP proteins are one of the major intrinsic proteins which comprise the family of important membrane channel proteins [44]. NIPs are categorised into three main groups, namely, NIP-I, NIP-II and NIP-III, with regard to the common substrate selectivity and consistency of amino acid composition [45]. The NIP-II group (such as OsNIP3;1, AtNIP5;1, AtNIP6;1 and ZmNIP3;1) has been found to be vital for the uptake and transporting of boron in several plants [44]. NIP-III group members (such as OsNIP2;1, OsNIP2;2, HvNIP2;1, HvNIP2;2 and CmNIP2;1) are revealed to be vital for the effectual uptake and translocation of Si [46]. A family of 10 NIP proteins is found in rice. Bienert et al. [47] reported that NIPs in Oryza sativa L., OsNIP2;1 (Lsi1) and OsNIP3;2 (Lsi2) are capable of facilitating an influx of AsIII into rice root cells.

2.2. Uptake of Organic Arsenic

Methylated As species, namely, MMA (CH3AsO(OH)2) and DMA ((CH3)2AsOOH), might be present in soil due to microbial actions or past usage of methylated As compounds, cacodylic acid or sodium salt of MMA and DMA as pesticides [42]. Microorganisms in soil may convert As species from AsV to AsIII and further to MMA and DMA. Suriyagoda et al. [48] stated that DMA and MMA might be taken up by the silicic acid transporter Lsi1. Plant roots are capable of taking up DMA and MMA, but the amounts of uptake are lower than those of inorganic As species and diminish with increasing numbers of methyl groups [49]. MMA(V) is partially reduced to trivalent MMA(III) in rice roots, but only MMA(V) is translocated to shoots [50]. DMA(V) is mobile in plants and may easily transfer from root to shoot. Muehe et al. [51] explained that methylated As is taken up gradually into rice relative to inorganic species but that it is freely translocated to grains.

2.3. Arsenic Species Translocation from Root to Shoot

The average translocation factor for As is around 0.8, which is higher than the other crops, such as barley (0.2) and wheat (0.1) [52].
As mentioned previously, the Si transporter OsNIP2;1 (Lsi1) is responsible for AsIII uptake, and Lsi2 drives AsIII efflux from rice root cells to the xylem [53]. Lsi1 is located in the distal side of the plasma membranes in exodermal and endodermal cells and is in charge of the influx of AsIII, whilst Lsi2 is located in the proximal sides of the same root cells and is in charge of the efflux of AsIII [54]. In other words, the synergy of Lsi1 and Lsi2 transports Si and AsIII into root cells. Si and AsIII in the xylem vessel are transported to the shoot via transpiration flow by Lsi1 and Lsi2 first and then by Lsi6, which is localised in the xylem parenchyma cells of leaves [55]. Detmann et al. [56] stated that the Lsi6 gene plays a vital role in the distribution of Si, or maybe AsIII, in rice shoot.
In rice, 13 Pi transporter genes (OsPT) can transport AsV to the root. Amongst these genes, OsPT1, OsPT2, OsPT4, OsPT6, OsPT8, OsPT9 and OsPT10 have a role in P uptake and translocation in rice. Certain Pi transporters also mediate AsV uptake [57]. Amongst these OsPTs, OsPT1 is thoroughly stated in roots and is a main regulator of Pi. OsPT2 has a vital role in Pi transferring from the root to the shoot [58]. AsV may be reduced to AsIII inside the rice root, and AsIII may then enter the xylem via a silicic acid/AsIII effluxer [59]. Chen et al. [60] explained that AsV may be quickly reduced to AsIII in plant cells by high As content 1 (HAC1) AsV reductases. Chao et al. [61] reported that HAC1 is vital in the reduction of AsV activity in the outer layer of the root (epidermis) and the inner layer adjacent to the xylem (pericycle).
Mitra et al. [14] expressed that DMA and MMA enter the NIP protein. However, AsIII is more capably taken up by roots than MMA and DMA. Zhao et al. [49] stated that the transferring from roots to shoots commonly rises with the rising quantity of methyl groups in As. DMA is extremely mobile throughout the xylem and phloem in rice. Tang et al. [62] reported that OsPTR7 may interact in the transferring of DMA in the phloem or xylem. High mobility of DMA occurs in the moving from roots to shoots and from leaves to grain.

2.4. Phloem and Xylem-Derived Pathways of As Species and As Loading in Grains

As may be transferred from roots to shoots through the xylem [48]. Phloem transportation is probably responsible for 54%, 56%, 100% and 89% of AsIII, AsV, MMA(V) and DMA(V) translocation into rice grains, respectively. In the phloem, organic arsenics are more transportable than inorganic arsenics [63]. Moreover, AsIII is transported to rice grains principally through the phloem pathway, whereas DMA is translocated to rice grains through the xylem and phloem pathways [62]. In arabidopsis, Duan et al. [64] reported that AtINT2 and AtINT4 (inositol transporters) may have a role in AsIII entering into the phloem and in adjusting the accumulation of As(III) in seeds. Hence, similar transporters in rice plants may be responsible for As(III) transport. Furthermore, OsPTR7 has a role in the long-distance transferring of DMA and in the accumulation of DMA in rice grains [62].

2.5. Phytotoxicity of Arsenic and Arsenic Detoxification Mechanism in Rice Plants

As is extremely phytotoxic to plants as it diminishes plant growth and crop yield [18]. Several rice varieties were subjected to AsIII and AsV by Shakoor et al. [67]. Seed germination was slightly limited at 0.5 and 1 mg·L−1, and a diminishing of around 10% in germination was detected at 2 mg·L−1. The growth of root was limited by 20% at 0.5 mg·L−1 of AsV. In addition, AsV was found to be more toxic than AsIII. The dangerous biochemical impact of As at the subcellular level is the production of reactive oxygen species (ROSs), such as hydroxyl radical (OH), superoxide radical (O2−) and hydrogen peroxide. ROSs are hazardous for plant metabolism and may lead to damage to macromolecules [68].
As previously mentioned, AsV is reduced to AsIII in plants. In addition, AsIII efflux to the external medium is a vital way of As detoxification in plants. Inside plant cells, AsIII may be detoxified by complexation with phytochelatins (PCs), followed by the accumulation of AsIII–PC complexes in vacuoles through OsABCC1 transporters [69]. OsABCC1 is one of the ATP-binding cassette (ABC) transporters. ABC transporter proteins play roles in the translocation of a broad range of substances within membranes using energy from ATP hydrolysis [70]. Song et al. [66] stated that OsABCC1 plays a vital role in the detoxification and decreasing As in rice grains.
HAC1 contributes to the defence against As in plants [71] and is essential for the efflux of AsIII from roots for AsV detoxification [72]. In rice, OsHAC1;1, OsHAC1;2 and OsHAC4 function as AsV reductase. Moreover, glutaredoxin possesses AsV reductase enzyme activity in maintaining the glutathione (GSH) pool and assists in AsIII efflux [73].
Brinke et al. [74] stated that with rising AsIII concentrations, the importance of the term ‘response to stress’ is replaced by the detoxification ways ‘glutathione biosynthesis’, which is related to the term ‘oxidation reduction’. GSH is applied as an electron donor by dehydroascorbate reductase to reconvert dehydroascorbate to ascorbate. GSH disulphide is the oxidised form of GSH, which may be reprocessed to GSH by glutathione reductase via reduced nicotinamide adenine dinucleotide phosphate. Hence, these different components of the ascorbate–GSH cycle may have a vital character in protecting cells against oxidative damage resulted by As toxicity [75].
After the reduction of AsV to AsIII, further mechanisms of detoxification arise in the vacuole via vacuolar sequestration. AsIII chelates with sulfhydryl (–SH)-rich protein and arranges a complex that is separated by vacuolar transporters (PCs). In rice, two phytochelatin synthase enzymes have been testified, comprising OsPCS1 and OsPCS2 [73].

3. Effects of Different Factors on Reducing Arsenic Uptake by Plants

Certain factors, such as pH, soil texture, organic matter (OM) and sulphide concentrations, may affect As uptake by plants [76]. Soil texture may affect As mobility due to differences in charges on the soil surface, which controls the adsorption and desorption procedures in soil. Soils with high amounts of clay have a higher As retention potential than coarse-textured soils. Reports also indicated that As uptake and concentrations are higher in plants grown in loamy sand than in plants grown in silty clay loam soils [77]. Moreover, As is five times more toxic in sand and loam than in clay soil, and its available form is a vital factor related to phytotoxicity [78].

3.1. Soil pH

pH is an important factor affecting As uptake [79]. An increase in pH commonly results in the mobilisation of As in soil. In general, an increase in soil pH results in a release of anions from within their exchange positions, along with AsV and AsIII [80]. Tu and Ma [79] reported that redox potential and pH influence As species. For example, under oxidising situations at pH < 6.9, H2AsO4− becomes the primary species, and at a high pH, HAsO42− is dominant. High soil pH (generally pH 8.5) increases the negative surface charges, such as hydroxyl ions, thereby facilitating the desorption of As from Fe oxides and the resulting mobilisation of As in the root area; these conditions, in turn, increase As accumulation in plants [14].

3.2. Soil Organic Matter

OM in soil may influence the mobility and bioavailability of As over redox reactions, anions (phosphate, DOC and silicate), As–OM complexation and competitive adsorption [81]. OM may also affect plant growth and As accumulation in rice plants. OM, theoretically, insolubilises As over certain mechanisms, such as the binding of As with phenolic OH, carboxylate and sulfhydryl groups with/without ternary complexes [82]. Norton et al. [83] stated that OM is important in the mobilisation of As from paddy fields because microbes utilising OM consume oxygen that results in a reduction in redox potential, which leads to As dissolution from FeOOH. Syu et al. [81] explained that the characteristics of soils and OMs should be considered before using OM amendments to As-polluted soils. The use of OM to As-polluted soils may exert different effects on the As accumulation and growth of rice plants [81]. For example, biochar may improve As reduction and release in flooded paddy soils [84], but augmenting farmyard manure to soils with high amounts of As leads to a reduction of plant growth [83]. Norton et al. [83] stated that OM may also play two other roles in As availability in soils: by desorbing As species from soil surface exchange sites and complexing As species with dissolved organic matter (DOM).

3.3. Concentration of Nitrogen, Phosphorous and Sulphate in Soil

In rice soils, the main form of nitrogen (N) is ammonium, whilst nitrate concentration is less than 10 μM. Rice roots discharge oxygen into the rhizosphere, thereby causing ammonium nitrification by microbes near the root surface [85]. The procedure of Fe redox cycling may be influenced by N cycling. The coupled NO3− reduction and Fe(II) oxidation can diminish As in paddy environments [63].
As previously mentioned, rice crops take up AsV via phosphate transporters [57]. Phosphate and arsenate are analogues and may compete for the same sorption sites on soil particles. The adding of phosphate commonly has two consequences: (i) raised downward move of As resulting in increased leaching from the topsoil and (ii) enhanced accessibility of As in the soil solution. AsV also acts as a phosphate analogue with respect to transport across the root plasma membrane [86]. Pigna et al. [87] reported that As toxicity in crops may be prevalent in situations where As pollution coexists with low available P.
Sulphur (S) is an element that interacts toughly with As, particularly under reducing conditions; the reduced forms of S can make a binding with As(III) [88]. Srivastava et al. [89] stated that S is important for plant growth as it regulates As tolerance over complexation of As by S-containing ligands (glutathione [GSH; γ-Glu-Cys-Gly] and PCs [GSH oligomers]). Zhang et al. [90] reported a reduction in translocating As from roots to shoots in high sulphate-pretreated rice plants.

3.4. Concentration of Iron and Manganese in Soil

Anwar et al. [9] expressed that Fe and Mn-rich compounds, such as goethite, ferruginous smectites, nontronite, pyrolusite and birnessite, absorb large amounts of As(V). Hence, As mobility may be low. A coating of Fe hydroxides/oxides identified as iron plaque, is normally formed on the roots of aquatic plant species. Iron plaque is the result of the oxidation of roots by releasing oxygen and oxidants into the rhizosphere [91,92]. Iron plaque also restrains the uptake of As by plants, possibly due to its adsorption or co-precipitation procedures [93]. Yu et al. [94] reported a negative correlation between As in rice grains and amorphous Fe oxide-bound As in soil and specified that amorphous Fe oxides might play a role as a barrier for As uptake by the plant. Liu et al. [91] expressed that Mn and Fe plaque can reduce the uptake of As in rice seedlings.

4. Agronomic Methods for Reducing Uptake and Accumulation of Arsenic by Plants

Awasthi et al. [12] stated three key plans to decrease As uptake by rice: (1) agronomic practices; (2) transforming the transporters involved in uptake; and (3) influencing the mobility of As in developing the synthesis of chelators.
For the agronomic strategy, researchers have tried to reduce As uptake by rice using different mitigation methods (Table 3). Several strategies are being practiced to mitigate As pollution, and they include overbreeding, bioremediation, transgenics and developed fertilisation; these techniques have their own limitations of time, ethics and applicability [95]. Using Fe oxides/hydroxides is one of the mitigation techniques to diminish As uptake by plants. Anwar et al. [9] reported that a high rate of goethite addition to soils may decrease As uptake by plants because goethite may adsorb As. Farquhar et al. [96] stated that As(V) oxyanions are toughly ‘sorbed’ to the surfaces of iron oxides such as goethite, hence, As uptake may be reduced by plants. Ultra et al. [92] stated that soil amendments with Am-FeOH can modify the accessibility of As uptake by rice plants irrigated with As-polluted water. The manipulation of Si is a way to abate As uptake by rice. This approach takes advantage of the fact that AsIII, the most prevalent As species in flooded porewater, shares the silicic acid uptake pathway in rice [97]. Liu et al. [98] reported that foliar using SiO2 nanoparticles in As-polluted paddy soil increases the dry weight of rice and obviously reduces As accumulation in grains and shoots. The addition of SiO2 nanoparticles increases pectin content and advances the mechanical force of the cell wall, resulting in decreased As uptake into rice cells [99]. Rice planted along with accumulators has received growing research attention due to the reduced As uptake by rice. Parveen et al. [100] stated that rice accompanied by accumulators in As-amended plots shows reduced As uptake in grains and shoots. Thus, certain accumulator plants, such as Pteris vittata, Vetiveria zizanioides and Phragmites australis, have been cultivated along with rice. The use of algae or bacteria to reduce As uptake by plants has also been reported [101]. Flooded rice fields offer ideal conditions for microbial and algal growth and regulate As bioavailability through precipitation, redox reactions, complexation and nutrient availability [95].
As shown in Table 3, using microalgae and bacteria are efficient in reducing As accumulation in rice.

5. Conclusions

Rice is a major dietary source of As; therefore, researchers have tried to reduce As uptake by rice plants. In the present study, several research papers were reviewed to investigate the journey of arsenic in rice. The key conclusions of the present study are as follows:
  • The accumulation of As in soils in Bangladesh (51,900 µg/L in root) and Taiwan (157,000 µg/L in root) is higher than that in other countries.
  • AsV enters the root via Pi transporters, and AsIII, DMA and MMA enter the root through NIPs.
  • AsV can be reduced to AsIII by HAC1. In addition, DMA is more mobile than other As species.
  • Soil properties, such as pH, OM and the amounts of Fe, Mn, N, P and S, can affect As uptake by rice.
  • Amongst the agronomic strategies for reducing the uptake and accumulation of As in rice, the use of microalgae and bacteria is the most efficient.

Author Contributions

T.A. was responsible for writing the initial draft of the manuscript. A.M. modified the manuscript and contributed to the literature search. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the Institute of Scientific Research Amin-Azma grant with the reference number A20191.

Acknowledgments

The authors would like to express their gratitude to the Institute of Scientific Research Amin-Azma.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Hoang, T.V.; Xuan, V.K.T.; Rahman, M.M.; Choi, S.H.; Jeon, J.S. Heat stress transcription factor OsSPL7 plays a critical role in reactive oxygen species balance and stress responses in rice. Plant Sci. 2019, 289, 110273. [Google Scholar] [CrossRef]
  2. Mousavian, M.T.H.; Karizaki, V.M. Determination of Mass Transfer Parameters during Deep Fat Frying of Rice Crackers. Rice Sci. 2012, 19, 64–69. [Google Scholar] [CrossRef]
  3. Ma, X.; Han, B.; Tang, J.; Zhang, J.; Cui, D.; Geng, L.; Zhou, H.; Li, M.; Han, L. Construction of chromosome segment substitution lines of Dongxiang common wild rice (Oryza rufipogon Griff.) in the background of the japonica rice cultivar Nipponbare (Oryza sativa L.). Plant Physiol. Biochem. 2019, 144, 274–282. [Google Scholar] [CrossRef] [PubMed]
  4. Pathaichindachote, W.; Panyawut, N.; Sikaewtung, K.; Patarapuwadol, S.; Muangprom, A. Genetic Diversity and Allelic Frequency of Selected Thai and Exotic Rice Germplasm Using SSR Markers. Rice Sci. 2019, 26, 393–403. [Google Scholar] [CrossRef]
  5. Chen, Y.; Han, Y.H.; Cao, Y.; Zhu, Y.G.; Rathinasabapathi, B.; Ma, L.Q. Arsenic Transport in Rice and Biological Solutions to Reduce Arsenic Risk from Rice. Front. Plant Sci. 2017, 8, 268. [Google Scholar] [CrossRef] [Green Version]
  6. Kobya, M.; Soltani, R.D.C.; Omwene, P.I.; Khataee, A. A review on decontamination of arsenic-contained water by electrocoagulation: Reactor configurations and operating cost along with removal mechanisms. Environ. Technol. Innov. 2020, 17, 100519. [Google Scholar] [CrossRef]
  7. Sodhi, K.K.; Kumar, M.; Agrawal, P.K.; Singh, D.K. Perspectives on arsenic toxicity, carcinogenicity and its systemic remediation strategies. Environ. Technol. Innov. 2019, 16, 100462. [Google Scholar] [CrossRef]
  8. Rahaman, M.S.; Akter, M.; Rahman, M.M.; Sikder, M.T.; Hosokawa, T.; Saito, T.; Kurasaki, M. Investigating the protective actions of D-pinitol against arsenic-induced toxicity in PC12 cells and the underlying mechanism. Environ. Toxicol. Pharm. 2020, 74, 103302. [Google Scholar] [CrossRef]
  9. Anwar, H.M.; Rengel, Z.; Damon, P.; Tibbett, M. Arsenic-phosphorus interactions in the soil-plant-microbe system: Dynamics of uptake, suppression and toxicity to plants. Environ. Pollut. 2018, 233, 1003–1012. [Google Scholar] [CrossRef]
  10. Yun, S.W.; Kim, D.H.; Kang, D.H.; Son, J.; Lee, S.Y.; Lee, C.K.; Lee, S.H.; Ji, W.H.; Baveye, P.C.; Yu, C. Effect of farmland type on the transport and spatial distribution of metal(loid)s in agricultural lands near an abandoned gold mine site: Confirmation of previous observations. J. Geochem. Explor. 2017, 181, 129–137. [Google Scholar] [CrossRef]
  11. Shrivastava, A.; Barla, A.; Majumdar, A.; Singh, S.; Bose, S. Arsenic mitigation in rice grain loading via alternative irrigation by proposed water management practices. Chemosphere 2020, 238, 124988. [Google Scholar] [CrossRef] [PubMed]
  12. Awasthi, S.; Chauhan, R.; Srivastava, S.; Tripathi, R.D. The Journey of Arsenic from Soil to Grain in Rice. Front. Plant Sci. 2017, 8, 1007. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Li, N.; Wang, J.; Song, W.Y. Arsenic Uptake and Translocation in Plants. Plant Cell Physiol. 2016, 57, 4–13. [Google Scholar] [CrossRef] [Green Version]
  14. Mitra, A.; Chatterjee, S.; Moogouei, R.; Gupta, D.K. Arsenic Accumulation in Rice and Probable Mitigation Approaches: A Review. Agronomy 2017, 7, 67. [Google Scholar] [CrossRef]
  15. Kabir, M.S.; Salam, M.A.; Paul, D.N.R.; Hossain, M.I.; Rahman, N.M.F.; Aziz, A.; Latif, M.A. Spatial Variation of Arsenic in Soil, Irrigation Water, and Plant Parts: A Microlevel Study. Sci. World J. 2016, 2186069. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Chakma, S.; Rahman, M.M.; Islam, P.; Awal, M.A.; Roy, U.K.; Haq, M.R. Arsenic in rice and rice straw. Bangladesh Vet. 2012, 29, 1–6. [Google Scholar] [CrossRef] [Green Version]
  17. Rahman, M.A.; Hasegawa, H.; Rahman, M.M.; Rahman, M.A.; Miah, M.A.M. Accumulation of arsenic in tissues of rice plant (Oryza sativa L.) and its distribution in fractions of rice grain. Chemosphere 2007, 69, 942–948. [Google Scholar] [CrossRef] [Green Version]
  18. Islam, S.; Rahman, M.M.; Islam, M.R.; Naidu, R. Geographical variation and age-related dietary exposure to arsenic in rice from Bangladesh. Sci. Total Environ. 2017, 601, 122–131. [Google Scholar] [CrossRef]
  19. Shah, A.L.; Naher, U.A.; Hasan, Z.; Islam, S.M.M.; Rahman, M.S.; Panhwar, Q.A.; Shamshuddin, J. Arsenic Management in Contaminated Irrigation Water for Rice Cultivation. Trop. Agric. Sci. 2016, 39, 155–166. [Google Scholar]
  20. Ma, L.; Wang, L.; Jia, Y.; Yang, Z. Arsenic speciation in locally grown rice grains from Hunan Province, China: Spatial distribution and potential health risk. Sci. Total Environ. 2016, 557, 438–444. [Google Scholar] [CrossRef]
  21. Li, J.; Dong, F.; Lu, Y.; Yan, Q.; Shim, H. Mechanisms Controlling Arsenic Uptake in Rice Grown in Mining Impacted Regions in South China. PLoS ONE 2014, 9, e108300. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. 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. Sci. China Chem. 2015, 58, 1898–1905. [Google Scholar] [CrossRef]
  23. Lu, Y.; Dong, F.; Deacon, C.; Chen, H.J.; Raab, A.; Meharg, A.A. Arsenic accumulation and phosphorus status in two rice (Oryza sativa L.) cultivars surveyed from fields in South China. Environ. Pollut. 2010, 158, 1536–1541. [Google Scholar] [CrossRef]
  24. Lin, S.C.; Chang, T.K.; Huang, W.D.; Lur, H.S.; Shyu, G.S. Accumulation of arsenic in rice plant: A study of an arsenic-contaminated site in Taiwan. Paddy Water Environ. 2015, 13, 11–18. [Google Scholar] [CrossRef]
  25. Patel, K.S.; Shirvas, K.; Brandt, R.; Jakubowski, N.; Hoffmann, P. Arsenic contamination in water, soil, sediment and rice of central India. Environ. Geochem. Health 2005, 27, 131–145. [Google Scholar] [CrossRef] [PubMed]
  26. Singh, V.; Brar, M.S.; Sharma, P.; Malhi, S.S. Arsenic in water, soil and rice plants in the Indo-Gangetic Plains of Northwestern India. Commun. Soil Sci. Plant Anal. 2010, 41, 1350–1360. [Google Scholar] [CrossRef]
  27. Bhattacharya, P.; Samal, A.C.; Majumdar, J.; Santra, S.C. Arsenic Contamination in Rice, Wheat, Pulses, and Vegetables: A Study in an Arsenic Affected Area of West Bengal, India. Water Air Soil Pollut. 2010, 213, 3–13. [Google Scholar] [CrossRef]
  28. Sidhu, S.S.; Brar, J.S.; Biswas, A.; Banger, K.; Saroa, G.S. Arsenic Contamination in Soil–Water–Plant (Rice, Oryza sativa L.) Continuum in Central and Sub-mountainous Punjab, India. Bull. Environ. Contam. Toxicol. 2012, 89, 1046–1050. [Google Scholar] [CrossRef]
  29. Juen, L.L.; Aris, A.Z.; Ying, L.W.; Haris, H. Bioconcentration and Translocation Efficiency of Metals in Paddy (Oryza sativa): A Case Study from Alor Setar, Kedah, Malaysia. Sains Malays. 2014, 43, 521–528. [Google Scholar]
  30. Zulkafflee, N.S.; Redzuan, N.A.M.; Hanafi, Z.; Selamat, J.; Ismail, M.R.; Praveena, S.M.; Razis, A.F.A. Heavy Metal in Paddy Soil and its Bioavailability in Rice Using In Vitro Digestion Model for Health Risk Assessment. Int. J. Environ. Res. Public Health 2019, 16, 4769. [Google Scholar] [CrossRef] [Green Version]
  31. Ruangwises, S.; Saipan, P.; Tengjaroenku, B.; Ruangwises, N. Total and Inorganic Arsenic in Rice and Rice Bran Purchased in Thailand. J. Food Prot. 2012, 75, 771–774. [Google Scholar] [CrossRef] [PubMed]
  32. Kuramata, M.; Abe, T.; Matsumoto, S.; Ishikawa, S. Arsenic accumulation and speciation in Japanese paddy rice cultivars. Soil Sci. Plant Nutr. 2011, 57, 248–258. [Google Scholar] [CrossRef]
  33. Makino, T.; Ishikawa, S.; Murakami, M.; Arao, T. Spatial Distribution and Risk Management of Heavy Metal Contamination in Japan. In Proceedings of the Monsoon Asia Agro-Environmental Research Consortium (MARCO) Symposium, Tsukuba, Japan, 26–28 August 2015; Available online: https://www.naro.affrc.go.jp/archive/niaes/marco/marco2015/text/ws3-6_t_makino.pdf (accessed on 22 December 2019).
  34. 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: Implications for Human Health Risk. J. Agric. Food Chem. 2014, 62, 6016–6024. [Google Scholar] [CrossRef] [PubMed]
  35. Fransisca, Y.; Small, D.M.; Morrison, P.D.; Spencer, M.J.S.; Ball, A.S.; Jones, O.A.H. Assessment of arsenic in Australian grown and imported rice varieties on sale in Australia and potential links with irrigation practises and soil geochemistry. Chemosphere 2015, 138, 1008–1013. [Google Scholar] [CrossRef]
  36. Williams, P.N.; Villada, A.; Deacon, C.; Raab, A.; Figuerola, J.; Green, A.J.; Feldmann, J.; Meharg, A.A. Greatly Enhanced Arsenic Shoot Assimilation in Rice Leads to Elevated Grain Levels Compared to Wheat and Barley. Environ. Sci. Technol. 2007, 41, 6854–6859. [Google Scholar] [CrossRef]
  37. Sommella, A.; Deacon, C.; Norton, G.; Pigna, M.; Violante, A.; Meharg, A.A. Total arsenic, inorganic arsenic, and other elements concentrations in Italian rice grain varies with origin and type. Environ. Pollut. 2013, 181, 38–43. [Google Scholar] [CrossRef]
  38. Atiaga-Franco, O.L.; Otero, X.L.; Gallego-Picó, A.; Escobar-Castañeda, L.A.; Bravo-Yagüe, J.C.; Carrera-Villacrés, D. Analysis of total arsenic content in purchased rice from Ecuador. Czech J. Food Sci. 2019, 37, 1–7. [Google Scholar] [CrossRef]
  39. Mondal, D.; Periche, R.; Tineo, B.; Bermejo, L.A.; Rahman, M.M.; Siddique, A.B.; Rahman, M.A.; Solis, J.L.; Cruz, G.J.F. Arsenic in Peruvian rice cultivated in the major rice growing region of Tumbes river basin. Chemosphere 2020, 241, 125070. [Google Scholar] [CrossRef]
  40. Abedin, M.J.; Feldmann, J.; Meharg, A.A. Uptake Kinetics of Arsenic Species in Rice Plants. Plant Physiol. 2002, 128, 1120–1128. [Google Scholar] [CrossRef] [Green Version]
  41. Luan, M.; Liu, J.; Liu, Y.; Han, X.; Sun, G.; Lan, W.; Luan, S. Vacuolar Phosphate Transporter 1 (VPT1) Affects Arsenate Tolerance by Regulating Phosphate Homeostasis in Arabidopsis. Plant Cell Physiol. 2018, 59, 1345–1352. [Google Scholar] [CrossRef]
  42. Mishra, S.; Mattusch, J.; Wennrich, R. Accumulation and transformation of inorganic and organic arsenic in rice and role of thiol-complexation to restrict their translocation to shoot. Sci. Rep. 2017, 7, 40522. [Google Scholar] [CrossRef] [PubMed]
  43. Ye, Y.; Yuan, J.; Chang, X.; Yang, M.; Zhang, L.; Lian, X. The Phosphate Transporter Gene OsPht1;4 Is Involved in Phosphate Homeostasis in Rice. PLoS ONE 2015, 10, e0126186. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Pommerrenig, B.; Diehn, T.A.; Bienert, G.P. Metalloido-porins: Essentiality of Nodulin 26-like intrinsic proteins in metalloid transport. Plant Sci. 2015, 238, 212–227. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Mitani, N.; Yamaji, N.; Ma, J.F. Characterization of substrate specificity of a rice silicon transporter, Lsi1. Pflüg. Arch. Eur. J. Physiol. 2008, 456, 679–686. [Google Scholar] [CrossRef]
  46. Pommerrenig, B.; Diehn, T.A.; Bernhardt, N.; Bienert, D.; Mitani-Ueno, N.; Fuge, J.; Bieber, A.; Spitzer, C.; Bräutigam, A.; Ma, J.F.; et al. Functional evolution of nodulin 26-like intrinsic proteins: From bacterial arsenic detoxification to plant nutrient transport. New Phytol. 2019, in press. [Google Scholar] [CrossRef] [Green Version]
  47. Bienert, G.P.; Thorsen, M.; Schüssler, M.D.; Nilsson, H.R.; Wagner, A.; Tamás, M.J.; Jahn, T.P. A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biol. 2008, 6, 26. [Google Scholar] [CrossRef] [Green Version]
  48. Suriyagoda, L.D.B.; Ditteret, K.; Lambers, H. Mechanism of arsenic uptake, translocation and plant resistance to accumulate arsenic in rice grains. Agric. Ecosyst. Environ. 2018, 253, 23–37. [Google Scholar] [CrossRef]
  49. Zhao, F.J.; Zhu, Y.G.; Meharg, A.A. Methylated Arsenic Species in Rice: Geographical Variation, Origin, and Uptake Mechanisms. Environ. Sci. Technol. 2013, 47, 3957–3966. [Google Scholar] [CrossRef]
  50. Guillod-Magnin, R.; Brüschweiler, B.J.; Aubert, R.; Haldimann, M. Arsenic species in rice and rice-based products consumed by toddlers in Switzerland. Food Addit. Contam. Part A 2018, 35, 1164–1178. [Google Scholar] [CrossRef] [Green Version]
  51. Muehe, E.M.; Wang, T.; Kerl, C.F.; Planer-Friedrich, B.; Fendorf, S. Rice production threatened by coupled stresses of climate and soil arsenic. Nat. Commun. 2019, 10, 4985. [Google Scholar] [CrossRef] [Green Version]
  52. Kalita, J.; Pradhan, A.K.; Shandilya, Z.M.; Tanti, B. Arsenic Stress Responses and Tolerance in Rice: Physiological, Cellular and Molecular Approaches. Rice Sci. 2018, 25, 235–249. [Google Scholar] [CrossRef]
  53. Ye, Y.; Li, P.; Xu, T.; Zeng, L.; Cheng, D.; Yang, M.; Luo, J.; Lian, X. OsPT4 Contributes to Arsenate Uptake and Transport in Rice. Front. Plant Sci. 2017, 8, 2197. [Google Scholar] [CrossRef] [Green Version]
  54. Zhao, F.J.; Ago, Y.; Mitani, N.; Li, R.L.; Sy, Y.H.; Yamaji, N.; McGrath, S.P.; Ma, J.F. The role of the rice aquaporin Lsi1 in arsenite efflux from roots. New Phytol. 2010, 186, 392–399. [Google Scholar] [CrossRef] [PubMed]
  55. Lin, Y.; Sun, Z.; Li, Z.; Xue, R.; Cui, W.; Sun, S.; Liu, T.; Zeng, R.; Song, Y. Deficiency in Silicon Transporter Lsi1 Compromises Inducibility of Anti-herbivore Defense in Rice Plants. Front. Plant Sci. 2019, 10, 652. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Detmann, K.C.; Araújo, W.L.; Martins, S.C.V.; Sanglard, L.M.V.; Reis, J.V.; Detmann, E.; Rodrigues, F.A.; Nunes-Nesi, A.; Fernie, A.R.; DaMatta, F.M. Silicon nutrition increases grain yield, which, in turn, exerts a feed-forward stimulation of photosynthetic rates via enhanced mesophyll conductance and alters primary metabolism in rice. New Phytol. 2012, 196, 752–762. [Google Scholar] [CrossRef] [Green Version]
  57. Cao, Y.; Sun, D.; Mei, H.; Liu, X.; Sun, S.; Xu, G.; Liu, Y.; Chen, Y. Knocking Out OsPT4 Gene Decreases Arsenate Uptake by Rice Plants and Inorganic Arsenic Accumulation in Rice Grains. Environ. Sci. Technol. 2017, 51, 12131–12138. [Google Scholar] [CrossRef]
  58. Yang, W.T.; Baek, D.; Yun, D.J.; Lee, K.S.; Hong, S.Y.; Bae, K.D.; Chung, Y.S.; Kwon, Y.S.; Kim, D.H.; Jung, K.H.; et al. Rice OsMYB5P improves plant phosphate acquisition by regulation of phosphate transporter. PLoS ONE 2018, 13, e0194628. [Google Scholar] [CrossRef]
  59. Carey, A.M.; Scheckel, K.G.; Lombi, E.; Newville, M.; Choi, Y.; Norton, G.J.; Charnock, J.M.; Feldmann, J.; Proce, A.H.; Meharg, A.A. Grain Unloading of Arsenic Species in Rice. Plant Physiol. 2010, 152, 309–319. [Google Scholar] [CrossRef] [Green Version]
  60. Chen, Y.; Sun, S.K.; Tang, Z.; Liu, G.; Moore, K.L.; Maathuis, J.M.; Miller, A.J.; McGrath, S.P.; Zhao, F.J. The Nodulin 26-like intrinsic membrane protein OsNIP3;2 is involved in arsenite uptake by lateral roots in rice. J. Exp. Bot. 2017, 68, 3007–3016. [Google Scholar] [CrossRef] [Green Version]
  61. Chao, D.Y.; Chen, Y.; Chen, J.; Shi, S.; Chen, Z.; Wang, C.; Danku, J.M.; Zhao, F.J. Genome-wide Association Mapping Identifies a New Arsenate Reductase Enzyme Critical for Limiting Arsenic Accumulation in Plants. PLoS ONE 2014, 12, e1002009. [Google Scholar] [CrossRef] [Green Version]
  62. Tang, Z.; Chen, Y.; Chen, F.; Ji, Y.; Zhao, F.J. OsPTR7 (OsNPF8.1), a Putative Peptide Transporter in Rice, is Involved in Dimethylarsenate Accumulation in Rice Grain. Plant Cell Physiol. 2017, 58, 904–913. [Google Scholar] [CrossRef] [PubMed]
  63. Kumarathilaka, P.; Seneweera, S.; Meharg, A.; Bundschuh, J. Arsenic accumulation in rice (Oryza sativa L.) is influenced by environment and genetic factors. Sci. Total Environ. 2018, 642, 485–496. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Duan, G.L.; Hu, Y.; Schneider, S.; McDermott, J.; Chen, J.; Sauer, N.; Rosen, B.P.; Daus, B.; Liu, Z.; Zhu, Y.G. Inositol transporters AtINT2 and AtINT4 regulate arsenic accumulation in Arabidopsis seeds. Nat. Plants 2016, 2, 15202. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Mosa, K.A.; Kumar, K.; Chhikara, S.; Mcdermott, J.; Liu, Z.; Musante, C.; White, J.C.; Dhankher, O.P. Members of rice plasma membrane intrinsic proteins subfamily are involved in arsenite permeability and tolerance in plants. Transgen. Res. 2012, 21, 1265–1277. [Google Scholar] [CrossRef]
  66. Song, W.Y.; Yamaki, T.; Yamaji, N.; Ko, D.; Jung, K.H.; Fujii-Kashino, M.; An, G.; Martinoia, E.; Lee, Y.; Ma, F.J. A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. PNAS 2014, 111, 15699–15704. [Google Scholar] [CrossRef] [Green Version]
  67. Shakoor, M.B.; Riaz, M.; Niazi, N.K.; Ali, S.; Rizwan, M.; Arif, M.S.; Arif, M. Chapter 18—Recent Advances in Arsenic Accumulation in Rice. In Advances in Rice Research for Abiotic Stress Tolerance; Hasanuzzaman, M., Fujita, M., Nahar, K., Biswas, J.K., Eds.; Elsevier: Amsterdam, The Netherlands, 2019. [Google Scholar] [CrossRef]
  68. Abbas, G.; Murtaza, B.; Bibi, I.; Shahid, M.; Niazi, N.K.; Khan, M.I.; Amjad, M.; Hussain, M. Arsenic Uptake, Toxicity, Detoxification, and Speciation in Plants: Physiological, Biochemical, and Molecular Aspects. Int. J. Environ. Res. Public Health 2018, 15, 59. [Google Scholar] [CrossRef] [Green Version]
  69. Sun, S.K.; Chen, Y.; Che, J.; Konishi, N.; Tang, Z.; Miller, A.J.; Ma, J.F.; Zhao, F.J. Decreasing arsenic accumulation in rice by overexpressing OsNIP1;1 and OsNIP3;3 through disrupting arsenite radial transport in roots. New Phytol. 2018, 219, 641–653. [Google Scholar] [CrossRef] [Green Version]
  70. Chang, Z.; Jin, M.; Yan, W.; Chen, H.; Qju, S.; Fu, S.; Xia, J.; Liu, Y.; Chen, Z.; Wu, J.; et al. The ATP-binding cassette (ABC) transporter OsABCG3 is essential for pollen development in rice. Rice 2018, 11, 58. [Google Scholar] [CrossRef]
  71. Meadows, R. How Plants Control Arsenic Accumulation. PLoS Biol. 2014, 12, e1002008. [Google Scholar] [CrossRef] [Green Version]
  72. Salt, D.E. Would the real arsenate reductase please stand up? New Phytol. 2017, 215, 1090–1101. [Google Scholar] [CrossRef] [Green Version]
  73. Shri, M.; Singh, P.K.; Kidiwai, M.; Gautam, N.; Dubey, S.; Verma, G.; Chakrabarty, D. Recent advances in arsenic metabolism in plants: Current status, challenges and highlighted biotechnological intervention to reduce grain arsenic in rice. Metallomics 2019, 11, 519–532. [Google Scholar] [CrossRef]
  74. Brinke, A.; Reifferscheid, G.; Klein, R.; Feiler, U.; Buchinger, S. Transcriptional changes measured in rice roots after exposure to arsenite-contaminated sediments. Environ. Sci. Pollut. Res. 2018, 25, 2707–2717. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  75. Jung, H.I.; Kong, M.S.; Lee, B.R.; Kim, T.H.; Cae, M.J.; Lee, E.J.; Jung, G.B.; Lee, C.H.; Sung, J.K.; Kim, Y.H. Exogenous Glutathione Increases Arsenic Translocation into Shoots and Alleviates Arsenic-Induced Oxidative Stress by Sustaining Ascorbate–Glutathione Homeostasis in Rice Seedlings. Front. Plant Sci. 2019, 10, 1089. [Google Scholar] [CrossRef] [PubMed]
  76. Hossain, K.; Quaik, S.; Pant, G.; Yada, S.; Maruthi, Y.A.; Rafatullah, M.; Nasir, M.; Ismail, N. Arsenic Fate in the Ground Water and its Effect on Soil-Crop Systems. Res. J. Environ. Toxicol. 2015, 9, 231–240. [Google Scholar] [CrossRef] [Green Version]
  77. Bakhat, H.F.; Zia, Z.; Abbas, S.; Hammad, H.M.; Shah, G.M.; Khalid, S.; Shahid, N.; Sajjad, M.; Fahad, S. Factors controlling arsenic contamination and potential remediation measures in soil-plant systems. Groundw. Sustain. Dev. 2019, 9, 100263. [Google Scholar] [CrossRef]
  78. Quazi, S.; Datta, R.; Sarkar, D. Effects of soil types and forms of arsenical pesticide on rice growth and development. Int. J. Environ. Technol. 2011, 8, 445–460. [Google Scholar] [CrossRef] [Green Version]
  79. Tu, S.; Ma, L.Q. Interactive effects of pH, arsenic and phosphorus on uptake of As and P and growth of the arsenic hyperaccumulator Pteris vittata L. under hydroponic conditions. Environ. Exp. Bot. 2003, 50, 243–251. [Google Scholar] [CrossRef]
  80. Moreno-Jiménez, E.; Esteban, E.; Peñalosa, J.M. The Fate of Arsenic in Soil-Plant Systems. In Reviews of Environmental Contamination and Toxicology; Whitacre, D.M., Ed.; Springer: Berlin, Germany, 2015. [Google Scholar] [CrossRef] [Green Version]
  81. Syu, C.H.; Wu, P.R.; Lee, C.H.; Juang, L.W.; Lee, D.Y. Arsenic phytotoxicity and accumulation in rice seedlings grown in arsenic-contaminated soils as influenced by the characteristics of organic matter amendments and soils. J. Plant Nutr. Soil Sci. 2019, 182, 60–71. [Google Scholar] [CrossRef] [Green Version]
  82. Suda, A.; Makino, T. Effect of organic amendments on arsenic solubilization in soils during long-term flooded incubation. Int. J. Environ. Sci. Technol. 2016, 13, 2375–2382. [Google Scholar] [CrossRef] [Green Version]
  83. Norton, G.J.; Adomako, E.E.; Deacon, C.M.; Carey, A.M.; Price, A.H.; Mehang, A.A. Effect of organic matter amendment, arsenic amendment and water management regime on rice grain arsenic species. Environ. Pollut. 2013, 177, 38–47. [Google Scholar] [CrossRef]
  84. Qiao, J.T.; Li, X.M.; Hu, M.; Li, F.; Young, L.Y.; Sun, W.; Huang, W.; Cui, J. Transcriptional Activity of Arsenic-Reducing Bacteria and Genes Regulated by Lactate and Biochar during Arsenic Transformation in Flooded Paddy Soil. Environ. Sci. Technol. 2018, 51, 61–70. [Google Scholar] [CrossRef] [PubMed]
  85. Srivastava, S.; Pathare, V.S.; Sounderajan, S.; Suprasanna, P. Nitrogen supply influences arsenic accumulation and stress responses of rice (Oryza sativa L.) seedlings. J. Hazard. Mater. 2019, 267, 599–606. [Google Scholar] [CrossRef] [PubMed]
  86. Abedin, M.J.; Cotter-Howells, J.; Meharg, A.A. Arsenic uptake and accumulation in rice (Oryza sativa L.) irrigated with contaminated water. Plant Soil 2002, 240, 311–319. Available online: https://www.jstor.org/stable/24121150 (accessed on 20 December 2019). [CrossRef]
  87. Pigna, M.; Cozzolino, V.; Caporale, A.G.; Mora, M.L.; Meo, V.D.; Jara, A.A.; Violante, A. Effects of Phosphorus Fertilization on Arsenic Uptake by Wheat Grown in Polluted Soils. J. Soil Sci. Plant Nutr. 2010, 14, 428–442. [Google Scholar] [CrossRef] [Green Version]
  88. Boye, K.; Lezama-Pacheco, J.; Fendorf, S. Relevance of Reactive Fe:S Ratios for Sulfur Impacts on Arsenic Uptake by Rice. Soils 2017, 1, 1. [Google Scholar] [CrossRef] [Green Version]
  89. Srivastava, S.; Akkarakaran, J.J.; Sounderajan, S.; Shrivastava, M.; Suprasanna, P. Arsenic toxicity in rice (Oryza sativa L.) is influenced by sulfur supply: Impact on the expression of transporters and thiol metabolism. Geoderma 2016, 270, 33–42. [Google Scholar] [CrossRef]
  90. Zhang, J.; Zhao, Q.Z.; Duan, G.L.; Huang, Y.C. Influence of sulphur on arsenic accumulation and metabolism in rice seedlings. Environ. Exp. Bot. 2011, 72, 34–40. [Google Scholar] [CrossRef]
  91. Liu, W.L.; Zhu, Y.G.; Smith, F.A. Effects of iron and manganese plaques on arsenic uptake by rice seedlings (Oryza sativa L.) grown in solution culture supplied with arsenate and arsenite. Plant Soil 2005, 277, 127–138. [Google Scholar] [CrossRef]
  92. Ultra, V.U.; Nakayama, A.; Tanaka, S.; Kang, Y.; Sakurai, K.; Iwasaki, K. Potential for the alleviation of arsenic toxicity in paddy rice using amorphous iron-(hydr)oxide amendments. Soil Sci. Plant Nutr. 2009, 55, 160–169. [Google Scholar] [CrossRef] [Green Version]
  93. Lee, C.H.; Hsieh, Y.C.; Lin, T.H.; Lee, D.Y. Iron plaque formation and its effect on arsenic uptake by different genotypes of paddy rice. Plant Soil 2013, 363, 231–241. [Google Scholar] [CrossRef]
  94. Yu, H.Y.; Li, F.B.; Liu, C.S.; Huang, W.; Liu, T.X.; Yu, W.M. Chapter Five—Iron Redox Cycling Coupled to Transformation and Immobilization of Heavy Metals: Implications for Paddy Rice Safety in the Red Soil of South China. Adv. Agron. 2016, 137, 279–317. [Google Scholar] [CrossRef]
  95. Srivastava, S.; Srivastava, S.; Bist, V.; Awashti, S.; Chauhan, R.; Chaudhry, V.; Singh, P.C.; Dwivedi, S.; Niranjan, A.; Agrawal, L.; et al. Chlorella vulgaris and Pseudomonas putida interaction modulates phosphate trafficking for reduced arsenic uptake in rice (Oryza sativa L.). J. Hazard. Mater. 2018, 351, 177–187. [Google Scholar] [CrossRef] [PubMed]
  96. Farquhar, M.L.; Charnock, J.M.; Livens, F.R.; Vaughan, D.J. Mechanisms of Arsenic Uptake from Aqueous Solution by Interaction with Goethite, Lepidocrocite, Mackinawite, and Pyrite:  An X-ray Absorption Spectroscopy Study. Environ. Sci. Technol. 2002, 36, 1757–1762. [Google Scholar] [CrossRef] [PubMed]
  97. Limmer, M.A.; Mann, J.; Amaral, D.C.; Vargas, R.; Seyfferth, A.L. Silicon-rich amendments in rice paddies: Effects on arsenic uptake and biogeochemistry. Sci. Total Environ. 2018, 624, 1360–1368. [Google Scholar] [CrossRef] [PubMed]
  98. Liu, C.; Wei, L.; Zhang, S.; Xu, X.; Li, F. Effects of nanoscale silica sol foliar application on arsenic uptake, distribution and oxidative damage defense in rice (Oryza sativa L.) under arsenic stress. RSC Adv. 2014, 4, 57227–57234. [Google Scholar] [CrossRef]
  99. Cui, J.; Li, Y.; Jin, Q.; Li, F. Silica nanoparticles inhibit arsenic uptake into rice suspension cells via improving pectin synthesis and the mechanical force of the cell wall. Environ. Sci. Nano 2019, in press. [Google Scholar] [CrossRef]
  100. Parveen, A.; Mehrotra, S.; Singh, N. Rice planted along with accumulators in arsenic amended plots reduced arsenic uptake in grains and shoots. Chemosphere 2017, 184, 1327–1333. [Google Scholar] [CrossRef]
  101. Markley, C.T.; Herbert, B.E. Modeling Phosphate Influence on Arsenate Reduction Kinetics by a Freshwater Cyanobacterium. Environ. Model. Assess. 2009, 15, 361–368. [Google Scholar] [CrossRef]
  102. Wang, Y.; Li, Y.Q.; Lv, K.; Cheng, J.J.; Chen, X.L.; Ge, Y.; Yu, X.Y. Soil microalgae modulate grain arsenic accumulation by reducing dimethylarsinic acid and enhancing nutrient uptake in rice (Oryza sativa L.). Plant Soil 2018, 430, 99–111. [Google Scholar] [CrossRef]
  103. Upadhyay, A.K.; Singh, N.K.; Singh, R.; Rai, U.N. Amelioration of arsenic toxicity in rice: Comparative effect of inoculation of Chlorella vulgaris and Nannochloropsis sp. on growth, biochemical changes and arsenic uptake. Ecotoxicol. Environ. Saf. 2016, 124, 68–73. [Google Scholar] [CrossRef]
  104. Xiao, A.W.; Li, W.C.; Ye, Z.H. The effect of plant growth-promoting rhizobacteria (PGPR) on arsenic accumulation and the growth of rice plants (Oryza sativa L.). Chemosphere 2020, 242, 125136. [Google Scholar] [CrossRef]
  105. Lakshmanan, V.; Shantharaj, D.; Li, G.; Seyfferth, A.L.; Sherrier, D.J.; Bais, H.P. A natural rice rhizospheric bacterium abates arsenic accumulation in rice (Oryza sativa L.). Planta 2015, 242, 1037–1050. [Google Scholar] [CrossRef] [PubMed]
  106. Nookongbut, P.; Kantachote, D.; Megharaj, M.; Naidu, R. Reduction in arsenic toxicity and uptake in rice (Oryza sativa L.) by As-resistant purple nonsulfur bacteria. Environ. Sci. Pollut. Res. 2018, 25, 36530–36544. [Google Scholar] [CrossRef] [PubMed]
  107. Dolphen, R.; Thiravetyan, P. Reducing arsenic in rice grains by leonardite and arsenic–resistant endophytic bacteria. Chemosphere 2019, 223, 448–454. [Google Scholar] [CrossRef] [PubMed]
  108. Ye, W.L.; Khan, M.A.; McGrath, S.P.; Zhao, F.J. Phytoremediation of arsenic contaminated paddy soils with Pteris vittata markedly reduces arsenic uptake by rice. Environ. Pollut. 2011, 159, 3739–3743. [Google Scholar] [CrossRef]
  109. Kumar, A.; Dixit, G.; Singh, A.P.; Dwivedi, S.; Srivastava, S.; Mishra, K.; Tripathi, R.D. Selenate mitigates arsenite toxicity in rice (Oryza sativa L.) by reducing arsenic uptake and ameliorates amino acid content and thiol metabolism. Ecotoxicol. Environ. Saf. 2016, 133, 350–359. [Google Scholar] [CrossRef]
  110. Wan, Y.; Camara, A.Y.; Huang, Q.; Yu, Y.; Wang, Q.; Li, H. Arsenic uptake and accumulation in rice (Oryza sativa L.) with selenite fertilization and water management. Ecotoxicol. Environ. Saf. 2018, 156, 67–74. [Google Scholar] [CrossRef]
  111. Fleck, A.T.; Mattusch, J.; Schenk, M.K. Silicon decreases the arsenic level in rice grain by limiting arsenite transport. J. Plant Nutr. Soil Sci. 2013, 176, 785–794. [Google Scholar] [CrossRef]
  112. Lin, L.; Gao, M.; Qiu, W.; Huang, Q.; Song, Z. Reduced arsenic accumulation in indica rice (Oryza sativa L.) cultivar with ferromanganese oxide impregnated biochar composites amendments. Environ. Pollut. 2017, 231, 479–486. [Google Scholar] [CrossRef]
  113. Mlangeni, A.T.; Perez, M.; Raab, A.; Krupp, E.M.; Norton, G.J.; Feldmann, J. Simultaneous stimulation of arsenic methylation and inhibition of cadmium bioaccumulation in rice grain using zero valent iron and alternate wetting and drying water management. Sci. Total Environ. 2019, in press. [Google Scholar] [CrossRef]
Table
Table 1. Arsenic found in rice plants around the world.
Table 1. Arsenic found in rice plants around the world.
Plant’s PartsAs (µg/Kg); Average or RangeRemarksAreaReference
Grains230* Boro riceSadar Upazila (subdistrict), Faridpur, Bangladesh[15]
Straw2890
Husk750
Grains235White riceComilla district, Bangladesh[16]
Straw1149
Grains600BRRI dhan28Satkhira district, Bangladesh[17]
Straw1700
Root46,300
Grains700BRRI hybrid dhan1
Straw1900
Root51,900
Grains78 ± 26White riceBarisal, Bangladesh[18]
185 ± 82 Chandpur, Bangladesh
189 ± 72 Comilla, Bangladesh
180 ± 65 Dhaka, Bangladesh
177 ± 52 Munshiganj, Bangladesh
210 ± 95 Narayanganj, Bangladesh
Grains170 to 260BoroBhanga and Faridpur in Bangladesh[19]
Straw390 to 3430
Whole grains20 to 130Oryza sativa var. kalijiraMATLAB, Bangladesh
Grains129.4White riceHuang, China[20]
Grains250 ± 51White riceRenhua, China[21]
Straw3300 ± 1300
Root25,600 ± 12,500
Grains280 ± 67White riceLechang, China[21]
Straw5800 ± 2800
Root35,000 ± 9400
Grains147IndicaFujian, China[22]
202IndicaGuangdong, China
302IndicaGuangxi, China
200IndicaYunnan, China
184IndicaChongqing, China
218IndicaSichuan, China
187JaponicaJiangsu, China
277IndicaZhejiang, China
309IndicaJiangxi, China
216JaponicaHenan, China
308IndicaHunan, China
246IndicaHubei, China
263IndicaAnhui, China
196JaponicaLiaoning, China
426JaponicaJilin, China
(Unpolished samples)
Grains0.127 to 0.275IndicaHuahang-Simiao, China[23]
Husk0.314 to 0.985
Shoot0.93 to 6.19
Root35.4 to 327.3
Grains230 ± 240Taikeng No. 8Gaudan Plan, Taiwan[24]
Straw4700 ± 1400
Root266,000 ± 98,000
Grain150 ± 50Tain Nan No. 11
Straw3200 ± 400
Root157,000 ± 27,000
* Rice TypesAmbagarh Chouki, India[25]
Husk432IR-64
147Culture
411Shyamla
415G. Gurmatia
235Masuri
167Purnima
144Mahamaya
446Kalinga
324Luchai
18Safari
Grains3.30 to 4.91** NR the rice speciesPunjab, India[26]
Straw7.30 to 9.89
Grains451Boro riceWest Bengal, India[27]
Grains334Aman rice
Grains8.78Oryza sativa L.Central and sub-mountainous Punjab, India[28]
Straw3.94
Grains290 ± 580Oryza sativaAlor Setar, Kedah, Malaysia[29]
Straw80 ± 150
Root23,100 ± 12,670
Grains189 to 541Oryza sativaBesut, Sekinchan, Tanjung Karang and Sabak Bernam; Malaysia[30]
Grains124 to 136Polished rice (White)Thailand[31]
186 to 198Brown rice (White)
832 to 963Rice bran (White)
(Samples collected from markets (Thailand-grown)
Grains107 to 166White riceJapan; Low-As soils[32]
Grains
Grains160Brown riceJapan (average of the country)[33]
Grains283 ± 18* White rice (organic)Australia (not specified)[34]
241 ± 07White rice (long-grain)
438 ± 23Brown rice (organic)
287 ± 03Brown rice (whole)
198 ± 41Brown rice (long-grain)
Samples collected from markets (Australian-grown)
Grains170 ± 30* MahatmaAustralia (not specified)[35]
100 ± 30Brown
120 ± 30White
90 ± 20Medium grain white
220 ± 20Sushi
220 ± 20Arborio
210 ± 30Medium grain Arborio
Samples collected from markets (Australian-grown)
Grains0.13Oryza sativaCalifornia, US[36]
Straw0.7
Grains0.2Oryza sativaArkansas, US[36]
Straw1.5
Grains230 ± 10* ArborioLombardia, Piemonte, Emilia Romagna, and Calabria in Italy[37]
230 ± 20Carnaroli
180 ± 10Ribe
200 ± 10Ribe/Roma parboiled
190 ± 10Roma
280 ± 30Vialone Nano
190 ± 30Originario
Grains0.32Oryza sativaCarmargue, France[36]
Straw10.2
Grains232 ± 21Brown riceGuayas, Ecuador[38]
174 ± 14White riceGuayas, Ecuador
186 ± 17White riceLos Rios, Ecuador
Samples collected from markets (Ecuadorian-grown)
Grains167.94 Around Tumbes river basin in Peru[39]
* Local name. ** NR: Not Reported.
Table
Table 2. Gene families involved in As uptake, transport and metabolism in rice.
Table 2. Gene families involved in As uptake, transport and metabolism in rice.
NameCategoryAs speciesRemarksReference
OsPT1P transporterAsVAsV transporter to root[57]
OsPT2P transporterAsVAsV transporter root to shoot[57]
OsNIP2;1 (Lsi1)NIPsAsIII, DMA, MMAAsIII, DMA and MMA transporter to root[63]
OsNIP2;2 (Lsi2)
OsNIP1;1
OsNIP3;1
OsNIP3;2
OsNIP3;3
OsPIP1;2PIP (plasma membrane intrinsic protein)AsIIIAsIII transport root to shoot[65]
OsPIP1;3
OsPIP2;4
OsPIP2;6
OsPIP2;7
OsNRAMP1NRAMP (natural resistance-associated macrophage protein)AsIIIAsIII transport root to shoot[5]
OsHAC1;1NIPsDMA, MMA, AsVDMA and MMA transporter to root[63]
OsHAC1;2 AsV reduction to AsIII in root
OsHAC4
OsNPF8;1 (OsPTR7)Putative Peptide TransporterDMATranslocation of DMA in plant, including xylem, phloem and grains[62]
OsABCC1ATP-binding cassette transporterAsDetoxifying[66]
Table
Table 3. Reported ways for reducing the uptake of As by rice plants.
Table 3. Reported ways for reducing the uptake of As by rice plants.
Decreasing of As UptakeMethodRemarksReference
43% to 70%Using Anabaena azotica (Microalgae)(i) Decreasing translocation of As from root to grains; (ii) decreasing DMA in grains and roots and (iii) enhancing nutrient uptake and rice growth[102]
40%Using Chlorella vulgaris and Nannochloropsis sp. (Microalgae)(i) Increasing root and shoot length and biomass and (ii) reduction in cellular toxicity and antioxidant enzyme[103]
48.1% to 77.7%Using Chlorella vulgaris (Microalgae) and Pseudomonas putida (Bacteria)(i) Reducing As accessibility; (ii) modulating the As uptake and (iii) enhancing detoxification mechanism.[95]
3.5% to 26.0%Using rhizobacteria (PGPR)(i) Improving rice growth and (ii) decreasing As accumulation[104]
79% (in shoots)Using Pantoea sp (Bacteria; EA106)(i) improving Fe uptake by root; (ii) decreasing As accumulation[105]
52.3% to 64.5%Using Rhodopseudomonas palustris C1 and Rubrivivax benzoatilyticus C31(Nonsulfur bacteria)(i) Improving the rice growth; (ii) increasing chlorophyll a and b and (iii) reducing As accumulation[106]
31% (in grains; just leonardite);Using leonardite + Bacillus pumilus, Pseudomonas sp and Bacillus thuringiensis(i) High efficiency of leonardite in adsorption of arsenic and (ii) increasing productivity and reducing arsenic in grains[107]
92 % (in grains; leonardite + Bacillus pumilus)
91% (in grains; leonardite + Pseudomonas sp)
91% (in grains; leonardite + Bacillus thuringiensis)
17% to 82% (in straw)Using Pteris vittata (Plant)(i) Decreasing phosphate extractable; (ii) decreasing methylated As in grains more than inorganic As[108]
22% to 58% (in grains)
179% (in root)Using selenium amendments(i) Enhancing the essential amino acids; and (ii) increasing non-protein thiols and phytochelatins in rice[109]
144% (in shoot)
46% (in straw)Using Si-rich amendments(i) Decreasing As accumulation and (ii) reducing CH4 emissions from soil[97]
27.5 (in grains)Using selenite fertilization(i) Decreasing the soil solution As in flooded condition; (ii) decreasing As uptake by rice in aerobic and (iii) decreasing the proportion of As in rice shoots.[110]
50% (straw, flag leaf and husk)Using silicon(i) Increasing the Si, Fe and P in soil solution[111]
68.9% to 78.3% (in grains)Using ferromanganese oxide and biochar(i) increasing the Fe and Mn plaque content and (ii) improving the biomass weight of the rice[112]
32% (in grains under low water)Using zero valent iron(i) Increasing percentage productive tillers and grain yield and (ii) reducing the cadmium bioaccumulation in rice grains[113]

Share and Cite

MDPI and ACS Style

Abedi, T.; Mojiri, A. Arsenic Uptake and Accumulation Mechanisms in Rice Species. Plants 2020, 9, 129. https://doi.org/10.3390/plants9020129

AMA Style

Abedi T, Mojiri A. Arsenic Uptake and Accumulation Mechanisms in Rice Species. Plants. 2020; 9(2):129. https://doi.org/10.3390/plants9020129

Chicago/Turabian Style

Abedi, Tayebeh, and Amin Mojiri. 2020. "Arsenic Uptake and Accumulation Mechanisms in Rice Species" Plants 9, no. 2: 129. https://doi.org/10.3390/plants9020129

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop