Arsenic Uptake, Transport, Accumulation in Rice and Prospective Abatement Strategies - A Review

Keywords: Arsenic, ingestion, rice, transporters, toxicology

Abstract

Recent reports claim that arsenic (As) toxicity affects millions of individuals worldwide. A significant problem for rice output and quality as well as for human health is the high content of arsenic (As), a non-essential poisonous metalloid, in rice grains. Therefore, substantial research has been done on the interactions between rice and As in recent years. As rice plants uptake at the root surface is impacted by factors like radical oxygen loss and iron plaque. The absorption and movement of various As species as well as the transfer to sub cellular compartments include a multitude of transporters, including phosphate transporters and aquaglyceroporins. As III and AsV are transported into the root by phosphate transporters and intrinsic channels that mimic nodulin 26. The silicic acid transporter may have a substantial impact on how methylated As, dimethylarsinic acid (DMA), and monomethylarsonic acid (MMA), enter the root. The issue of As contamination in rice is being addressed by researchers and practitioners to the best of their abilities. Making better plans may be aided by recent research on rice that explains the processes of arsenic ingestion, transportation, and metabolism at the rhizosphere. Common agronomic techniques, such as collecting rainwater for agricultural irrigation, using natural substances that aid in the methylation of arsenic, and biotechnology methods, may be investigated in an effort to lessen the uptake of arsenic by food crops. Innovative agronomic techniques and recent research findings on arsenic contamination in rice crops will be included in this review.

References

Abedi, T., & Mojiri, A. (2020). Arsenic uptake and accumulation mechanisms in rice species. Plants, 9(2), 129.

https://doi.org/10.3390/plants9020129

Abou-Shanab, R. A. I., Santelli, C. M., & Sadowsky, M. J. (2022). Bioaugmentation with As-transforming bacteria improves arsenic availability and uptake by the hyperaccumulator plant Pteris vittata (L). International Journal of Phytoremediation, 24(4), 420–428. https://doi.org/10.1080/15226514.2021.1951654

Adomako, E. E., Williams, P. N., Deacon, C., & Meharg, A. A. (2011). Inorganic arsenic and trace elements in Ghanaian grain staples. Environmental Pollution, 159(10), 2435–2442. https://doi.org/10.1016/j.envpol.2011.06.031

Ahoulé, D. G., Lalanne, F., Mendret, J., Brosillon, S., & Maïga, A. H. (2015). Arsenic in African Waters: A Review. Water, Air & Soil Pollution, 226(9), 302. https://doi.org/10.1007/s11270-015-2558-4

Anawar, H. M., Rengel, Z., Damon, P., & Tibbett, M. (2018). Arsenic-phosphorus interactions in the soil-plant-microbe system: Dynamics of uptake, suppression and toxicity to plants. Environmental Pollution, 233, 1003–1012. https://doi.org/10.1016/j.envpol.2017.09.098

Anyanwu, B., Ezejiofor, A., Igweze, Z., & Orisakwe, O. (2018). Heavy metal mixture exposure and effects in developing nations: An update. Toxics, 6(4), 65. https://doi.org/10.3390/toxics6040065

Arslan, B., Djamgoz, M. B. A., & Akün, E. (2016). Arsenic: A review on exposure pathways, accumulation, mobility and transmission into the human food chain. In Reviews of Environmental Contamination and Toxicology, pp. 27–51. https://doi.org/10.1007/398_2016_18

Awasthi, S., Chauhan, R., Srivastava, S., & Tripathi, R. D. (2017). The journey of arsenic from soil to grain in rice. Frontiers in Plant Science, 8. https://doi.org/10.3389/fpls.2017.01007

Bakhat, H. F., Zia, Z., Abbas, S., Hammad, H. M., Shah, G. M., Khalid, S., Shahid, N., Sajjad, M., & Fahad, S. (2019). Factors controlling arsenic contamination and potential remediation measures in soil-plant systems.Ground water for Sustainable Development, 9, 100263. https://doi.org/10.1016/j.gsd.2019.100263

Bakhat, H. F., Zia, Z., Fahad, S., Abbas, S., Hammad, H. M., Shahzad, A. N., Abbas, F., Alharby, H., & Shahid, M. (2017). Arsenic uptake, accumulation and toxicity in rice plants: Possible remedies for its detoxification: A review. Environmental Science and Pollution Research, 24(10), 9142–9158. https://doi.org/10.1007/s11356-017-8462-2

Banerjee, M., Banerjee, N., Bhattacharjee, P., Mondal, D., Lythgoe, P. R., Martínez, M., Pan, J., Polya, D. A., & Giri, A. K. (2013). High arsenic in rice is associated with elevated genotoxic effects in humans. Scientific Reports, 3(1), 2195. https://doi.org/10.1038/srep02195

Begum, M., & M. S. (2016). Effect of arsenic on photosynthesis and oxidative stress in rice (Oryza sativa L.) Indian Journals. Com, 51(1 to 3), 23–20.

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 and Water Environment, 8(1), 63–70. https://doi.org/10.1007/s10333-009-0180-z

Cao, Y., Sun, D., Ai, H., Mei, H., Liu, X., Sun, S., Xu, G., Liu, Y., Chen, Y., & Ma, L. Q. (2017). Knocking out OsPT4 Gene decreases arsenate uptake by rice plants and inorganic arsenic accumulation in rice grains. Environmental Science & Technology, 51(21), 12131–12138. https://doi.org/10.1021/acs.est.7b03028

Carbonell, A. A., Aarabi, M. A., DeLaune, R. D., Gambrell, R. P., & Patrick, W. H. (1998). Bioavailability and uptake of arsenic by wetland vegetation: Effects on plant growth and nutrition. Journal of Environmental Science and Health, Part A, 33(1), 45–66. https://doi.org/10.1080/10934529809376717

Carey, A.M., Scheckel, K. G., Lombi, E., Newville, M., Choi, Y., Norton, G. J., Charnock, J. M., Feldmann, J., Price, A. H., & Meharg, A. A. (2009). Grain unloading of arsenic species in rice. Plant Physiology, 152(1), 309–319.

https://doi.org/10.1104/pp.109.146126

Chatterjee, S., Mitra, A., Datta, S., & Vijay Veer, V.(2013). Phytoremediation protocols: an overview. Springer-Verlag Berlin Heidelberg, Plant-Based Remediation Processes, Vol. 1. pp.1–18.https://doi.org/10.1007/978-3-642-35564-6_1

Finnegan, P. M., & Chen, W. (2012). Arsenic toxicity: The effects on plant metabolism. Frontiers in Physiology, 3. https://doi.org/10.3389/fphys.2012.00182

Garg, N., & Singla, P. (2011). Arsenic toxicity in crop plants: physiological effects and tolerance mechanisms. Environmental Chemistry Letters, 9(3), 303–321. https://doi.org/10.1007/s10311-011-0313-7

Gupta, D. K., Srivastava, S., Huang, H. G., Romero-Puertas, M. C., &Sandalio, L. M. (2011). Arsenic tolerance and detoxification mechanisms in plants. In Detoxification of Heavy Metals, pp. 169–179. https://doi.org/10.1007/978-3-642-21408-0_9

Hele, A. K., & Moloro, H. B. (2023). Review on levels of some selected heavy metals in commercially available rice in Ethiopia. East African Scholars Journal of Agriculture and Life Sciences, 6(1), 15–28. https://doi.org/10.36349/easjals.2023.v06i01.002

Hernández, L. E., Sobrino-Plata, J., Montero-Palmero, M. B., Carrasco-Gil, S., Flores-Cáceres, M. L., Ortega-Villasante, C., & Escobar, C. (2015). Contribution of glutathione to the control of cellular redox homeostasis under toxic metal and metalloid stress. Journal of Experimental Botany, 66(10), 2901–2911. https://doi.org/10.1093/jxb/erv063

Howladar, M., Uddin, M., Islam, M., Parveen, Z., & Rahman, M. (2019). Effects of arsenic and phosphorus on the growth and nutrient concentration in rice plant. Journal of Biodiversity Conservation and Bioresource Management, 5(1), 31–38. https://doi.org/10.3329/jbcbm.v5i1.42183

Huang, J.H., Fecher, P., Ilgen, G., Hu, K.N., & Yang, J. (2012). Speciation of arsenite and arsenate in rice grain – Verification of nitric acid based extraction method and mass sample survey. Food Chemistry, 130(2), 453–459. https://doi.org/10.1016/j.foodchem.2011.07.059

Huang, Y., Chen, Z., & Liu, W. (2012). Influence of iron plaque and cultivars on antimony uptake by and translocation in rice (Oryza sativa L.) seedlings exposed to Sb(III) or Sb(V). Plant and Soil, 352(1–2), 41–49. https://doi.org/10.1007/s11104-011-0973-x

Islam, M.S., Rahman, M.M., & Paul, N.K. (2016). Arsenic-induced morphological variations and the role of phosphorus in alleviating arsenic toxicity in rice (Oryza sativa L.). Plant Science Archives, 1(1), 1–10.

Jia, Y., Huang, H., Zhong, M., Wang, F.H., Zhang, L.M., & Zhu, Y.G. (2013). Microbial arsenic methylation in soil and rice rhizosphere. Environmental Science & Technology, 47(7), 3141–3148. https://doi.org/10.1021/es303649v

Kamiya, T., Islam, R., Duan, G., Uraguchi, S., & Fujiwara, T. (2013). Phosphate deficiency signalling pathway is a target of arsenate and phosphate transporter OsPT1 is involved in As accumulation in shoots of rice. Soil Science and Plant Nutrition, 59(4), 580–590. https://doi.org/10.1080/00380768.2013.804390

Kobya, M., Soltani, R. D. C., Omwene, P. I., & Khataee, A. (2020). A review on decontamination of arsenic-contained water by electrocoagulation: Reactor configurations and operating cost along with removal mechanisms. Environmental Technology & Innovation, 17, 100519. https://doi.org/10.1016/j.eti.2019.100519

Koch, I., Dee, J., House, K., Sui, J., Zhang, J., McKnight-Whitford, A., & Reimer, K. J. (2013). Bio-accessibility and speciation of arsenic in country foods from contaminated sites in Canada. Science of The Total Environment, 449, 1–8. https://doi.org/10.1016/j.scitotenv.2013.01.047

Kumarathilaka, P., Seneweera, S., Meharg, A., & Bundschuh, J. (2018). Arsenic accumulation in rice (Oryza sativa L.) is influenced by environment and genetic factors. Science of The Total Environment, 642, 485–496. https://doi.org/10.1016/j.scitotenv.2018.06.030

Lakshmanan, V., Shantharaj, D., Li, G., Seyfferth, A. L., Janine Sherrier, D., & Bais, H. P. (2015). A natural rice rhizospheric bacterium abates arsenic accumulation in rice (Oryza sativa L.). Planta, 242(4), 1037–1050. https://doi.org/10.1007/s00425-015-2340-2

Lin, Y., Sun, Z., Li, Z., Xue, R., Cui, W., Sun, S., Liu, T., Zeng, R., & Song, Y. (2019). Deficiency in silicon transporter Lsi1 compromises inducibility of anti-herbivore defense in rice plants. Frontiers in Plant Science, 10.

https://doi.org/10.3389/fpls.2019.00652

Madrid-Delgado, G., Orozco-Miranda, M., Cruz-Osorio, M., Hernández-Rodríguez, O.A., Rodríguez-Heredia, R., Roa-Huerta, M., & Dolores Avila-Quezada, G. (2021).Pathways of phosphorus absorption and early signalling between the mycorrhizal fungi and plants. Phyton., 90(5), 1321–1338. https://doi.org/10.32604/phyton.2021.016174

Mallick, S., Sinam, G., & Sinha, S. (2011). Study on arsenate tolerant and sensitive cultivars of Zea mays L.: Differential detoxification mechanism and effect on nutrients status. Ecotoxicology and Environmental Safety, 74(5), 1316–1324. https://doi.org/10.1016/j.ecoenv.2011.02.012

Meharg, A. A., Williams, P. N., Adomako, E., Lawgali, Y. Y., Deacon, C., Villada, A., Cambell, R. C. J., Sun, G., Zhu, Y.G., Feldmann, J., Raab, A., Zhao, F.J., Islam, R., Hossain, S., & Yanai, J. (2009). Geographical variation in total and inorganic arsenic content of polished (white) rice. Environmental Science & Technology, 43(5), 1612–1617. https://doi.org/10.1021/es802612a

Mitra, A., Chatterjee, S., Moogouei, R., & Gupta, D. (2017). Arsenic accumulation in rice and probable mitigation approaches: A Review. Agronomy, 7(4), 67. https://doi.org/10.3390/agronomy7040067

Nath, S., Panda, P., Mishra, S., Dey, M., Choudhury, S., Sahoo, L., & Panda, S. K. (2014). Arsenic stress in rice: Redox consequences and regulation by iron. Plant Physiology and Biochemistry, 80, 203–210. https://doi.org/10.1016/j.plaphy.2014.04.013

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. Environmental Pollution, 177, 38–47. https://doi.org/10.1016/j.envpol.2013.01.049

Norton, G. J., Deacon, C. M., Xiong, L., Huang, S., Meharg, A. A., & Price, A. H. (2010). Genetic mapping of the rice genome in leaves and grain: identification of QTLs for 17 elements including arsenic, cadmium, iron and selenium. Plant and Soil, 329(1–2), 139–153. https://doi.org/10.1007/s11104-009-0141-8

Paola, S. G., Melina, A., Talano, Ana L.W.O., Sabrina, G.I., María, I.M., & Elizabeth, A. (2014). Update on mechanisms involved in arsenic and chromium accumulation, translocation and homeostasis in plants. Nova Science Publishers, In: Heavy Metal Remediation, Editors: Dharmendra Kumar Gupta and Soumya Chatterjee © 2014 Nova Science Publishers, Inc. Inc, pp. 45–72.

Pigna, M., Cozzolino, V., Giandonato Caporale, A., Mora, M. L., di Meo, V., Jara, A. A., &Violante, A. (2010). Effects of phosphorus fertilization on arsenic uptake by wheat grown in polluted soils. Journal of Soil Science and Plant Nutrition, 10(4), 428–442. https://doi.org/10.4067/S0718-95162010000200004

Quazi, S., Datta, R., & Sarkar, D. (2011). Effects of soil types and forms of arsenical pesticide on rice growth and development. International Journal of Environmental Science & Technology, 8(3), 445–460. https://doi.org/10.1007/BF03326231

Raab, A., Williams, P. N., Meharg, A., & Feldmann, J. (2007).Uptake and translocation of inorganic and methylated arsenic species by plants. Environmental Chemistry, 4(3), 197. https://doi.org/10.1071/EN06079

Rahman, M. A., Rahman, M. M., & Naidu, R. (2014). Arsenic in rice. Elsevier, In Wheat and Rice in Disease Prevention and Health, pp. 365–375. https://doi.org/10.1016/B978-0-12-401716-0.00028-3

Saha, J., Dutta, M., & Biswas, A. K. (2017). Influence of arsenate and phosphate on the regulation of growth and TCA Cycle in the rice (Oryza sativa L.) Cultivars IR 64 and Nayanmani. American Journal of Plant Sciences, 08(08), 1868–1887. https://doi.org/10.4236/ajps.2017.88127

Seyfferth, A. L., Webb, S. M., Andrews, J. C., & Fendorf, S. (2010). Arsenic localization, speciation, and co-occurrence with iron on rice (Oryza sativa L.) roots having variable Fe coatings. Environmental Science & Technology, 44(21), 8108–8113. https://doi.org/10.1021/es101139z

Sharma, I. (2012). Arsenic induced oxidative stress in plants. Biologia, 67(3), 447–453. https://doi.org/10.2478/s11756-012-0024-y

Shi, S., Wang, T., Chen, Z., Tang, Z., Wu, Z., Salt, D. E., Chao, D.Y., & Zhao, F.J. (2016). OsHAC1;1 and OsHAC1;2 Function as arsenate reductases and regulate arsenic accumulation. Plant Physiology, 172(3), 1708–1719. https://doi.org/10.1104/pp.16.01332

Song, W.-Y., Yamaki, T., Yamaji, N., Ko, D., Jung, K.-H., Fujii-Kashino, M., An, G., Martinoia, E., Lee, Y., & Ma, J. F. (2014). A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. Proceedings of the National Academy of Sciences, 111(44), 15699–15704. https://doi.org/10.1073/pnas.1414968111

Srivastava, S., Akkarakaran, J. J., Sounderajan, S., Shrivastava, M., & Suprasanna, P. (2016). Arsenic toxicity in rice (Oryza sativa L.) is influenced by sulphur supply: Impact on the expression of transporters and thiol metabolism. Geoderma, 270, 33–42. https://doi.org/10.1016/j.geoderma.2015.11.006

Srivastava, S., Pathare, V. S., Sounderajan, S., &Suprasanna, P. (2019). Nitrogen supply influences arsenic accumulation and stress responses of rice (Oryza sativa L.) seedlings. Journal of Hazardous Materials, 367, 599–606. https://doi.org/10.1016/j.jhazmat.2018.12.121

Srivastava, S., Srivastava, S., Bist, V., Awasthi, S., Chauhan, R., Chaudhry, V., Singh, P. C., Dwivedi, S., Niranjan, A., Agrawal, L., Chauhan, P. S., Tripathi, R. D., & Nautiyal, C. S. (2018). Chlorella vulgaris and Pseudomonas putida interaction modulates phosphate trafficking for reduced arsenic uptake in rice (Oryza sativa L.). Journal of Hazardous Materials, 351, 177–187. https://doi.org/10.1016/j.jhazmat.2018.02.039

Strawn, D. G. (2018). Review of interactions between phosphorus and arsenic in soils from four case studies. Geochemical Transactions, 19(1), 10. https://doi.org/10.1186/s12932-018-0055-6

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. Environmental Pollution, 159(4), 947–953. https://doi.org/10.1016/j.envpol.2010.12.016

Syu, C.H., Wu, P.R., Lee, C.H., Juang, K.W., & Lee, D.Y.(2019). Arsenic phytotoxicity and accumulation in rice seedlings grown in arsenic contaminated soils as influenced by the characteristics of organic matter amendments and soils. Journal of Plant Nutrition and Soil Science, 182 (1), 60–71. https://doi.org/10.1002/jpln.201800337

Thakur, S., Singh, L., Wahid, Z. A., Siddiqui, M. F., Atnaw, S. M., & Din, M. F. M. (2016). Plant-driven removal of heavy metals from soil: uptake, translocation, tolerance mechanism, challenges, and future perspectives. Environmental Monitoring and Assessment, 188(4), 206. https://doi.org/10.1007/s10661-016-5211-9

Ultra, V. U., Nakayama, A., Tanaka, S., Kang, Y., Sakurai, K., & Iwasaki, K. (2009). Potential for the alleviation of arsenic toxicity in paddy rice using amorphous iron-hydroxide amendments. Soil Science and Plant Nutrition, 55(1), 160–169. https://doi.org/10.1111/j.1747-0765.2008.00341.x

Wang, P., Zhang, W., Mao, C., Xu, G., & Zhao, F.-J. (2016). The role of OsPT8 in arsenate uptake and varietal difference in arsenate tolerance in rice. Journal of Experimental Botany, 67(21), 6051–6059. https://doi.org/10.1093/jxb/erw362

Wang, X., Peng, B., Tan, C., Ma, L., & Rathinasabapathi, B. (2015). Recent advances in arsenic bioavailability, transport, and speciation in rice. Environmental Science and Pollution Research, 22(8), 5742–5750. https://doi.org/10.1007/s11356-014-4065-3

Williams, P. N., Raab, A., Feldmann, J., & Meharg, A. A. (2007). Market basket survey shows elevated levels of As in South Central U.S. processed rice compared to California: Consequences for human dietary exposure. Environmental Science & Technology, 41(7), 2178–2183. https://doi.org/10.1021/es061489k

Xu, J., Shi, S., Wang, L., Tang, Z., Lv, T., Zhu, X., Ding, X., Wang, Y., Zhao, F., & Wu, Z. (2017). OsHAC4 is critical for arsenate tolerance and regulates arsenic accumulation in rice. New Phytologist., 215(3), 1090–1101. https://doi.org/10.1111/nph.14572

Yang, J., Gao, M., Hu, H., Ding, X., Lin, H., Wang, L., Xu, J., Mao, C., Zhao, F., & Wu, Z. (2016). OsCLT1, a CRT like transporter 1, is required for glutathione homeostasis and arsenic tolerance in rice. New Phytologist, 211(2), 658–670. https://doi.org/10.1111/nph.13908

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., & Kim, D. H. (2018). Rice OsMYB5P improves plant phosphate acquisition by regulation of phosphate transporter. PLOS ONE, 13(3), e0194628. https://doi.org/10.1371/journal.pone.0194628

Ye, Y., Li, P., Xu, T., Zeng, L., Cheng, D., Yang, M., Luo, J., & Lian, X. (2017). OsPT4 contributes to arsenate uptake and transport in rice. Frontiers in Plant Science, 8. https://doi.org/10.3389/fpls.2017.02197

Yu, H.Y., Li, F.B., Liu, C.S., Huang, W., Liu, T.X., & Yu, W.M. (2016). Iron redox cycling coupled to transformation and immobilization of heavy metals: Implications for paddy rice safety in the red soil of South China. In Advances in Agronomy, pp. 279–317. https://doi.org/10.1016/bs.agron.2015.12.006

Zhang, J., Zhao, Q.Z., Duan, G.L., & Huang, Y.C. (2011). Influence of sulphur on arsenic accumulation and metabolism in rice seedlings. Environmental and Experimental Botany, 72(1), 34–40. https://doi.org/10.1016/j.envexpbot.2010.05.007

Zhao, F., Ago, Y., Mitani, N., Li, R., Su, Y., Yamaji, N., McGrath, S. P., & Ma, J. F. (2010).The role of the rice aquaporin Lsi1 in arsenite efflux from roots. New Phytologist, 186(2), 392–399. https://doi.org/10.1111/j.1469-8137.2010.03192.x

Zhao, F.-J., Zhu, Y.-G., & Meharg, A. A. (2013). Methylated arsenic species in rice: Geographical variation, origin, and uptake mechanisms. Environmental Science & Technology, 47(9), 3957–3966. https://doi.org/10.1021/es304295n

Zhao, X. Q., Mitani, N., Yamaji, N., Shen, R. F., & Ma, J. F. (2010). Involvement of silicon influx transporter OsNIP2;1 in Selenite uptake in rice. Plant Physiology, 153(4), 1871–1877. https://doi.org/10.1104/pp.110.157867

Zheng, M.Z., Li, G., Sun, G.-X., Shim, H., & Cai, C.(2013). Differential toxicity and accumulation of inorganic and methylated arsenic in rice. Plant and Soil, 365(1–2), 227–238. https://doi.org/10.1007/s11104-012-1376-3

Published
2023-04-30
How to Cite
Bera, A., & Choudhury, B. (2023). Arsenic Uptake, Transport, Accumulation in Rice and Prospective Abatement Strategies - A Review. International Journal of Experimental Research and Review, 30, 388-401. https://doi.org/10.52756/ijerr.2023.v30.036
Section
Articles