Differential responses of two Iranian rice cultivars to arsenite toxicity

Document Type: Original Article


1 Department of Plant Biology, Faculty of Biological Science, Tarbiat Modares University, Tehran, Iran

2 Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden



Arsenic (As) is a toxic metalloid which is usually found in rice fields as a contamination and has negative effects on the plant growth and reduces the crop yield. Similar to heavy metals, the deleterious effects of As may be due to, at least in part, the amount of absorbed As and disturbance of the plant water status. In this connection, different varieties of the same species may show differential performances. Comparative responses to 75 µM AsIII were evaluated in two Iranian rice cultivars adapted to moderate-humid vs. very warm and dry climates (Hashemi and Amber, respectively). Although both cultivars absorbed AsIII, but its translocation factor was lower in Amber accompanied by accumulation of soluble sugars and glycine betaine and lower level of internal ABA. Moreover, adverse effect of AsIII onrelative water content and stomata closure was less prominent in Amber, compared to Hashemi. Results suggest that cultivars adapted to dry conditions are more capable to withstand against As and to control its entrance to human food chain.


Abedin, M. J. and A. A.Meharg, 2002.' Relative toxicity of arsenite and arsenate on germination and early seedling growth of rice (Oryza sativa L.)'. Plant Soil, 243: 57–66.

Ahmed, Z. U., G. M. Panaullah, H. Gauch, S. R. McCouch, W. Tyagi, M. S. Kabir and J. M. Duxbury, 2011. 'Genotype and environment effects on rice (Oryza sativa L.) grain arsenic concentration in Bangladesh'. Plant Soil 338: 367-382.

Anjum, S.A., M. Tanveer, S. Hussain, B. Shahzad, U. Ashraf, S. Fahad, W. Hassan, S. Jan, I. Khan, M. F. Saleem, A. A. Bajwa, L. Wang, A. Mahmood, R. A. Samad and S. A. Tung, 2016.' Osmoregulation and antioxidant production in maize under combined cadmium and arsenic stress'. Environmental Science and Pollution Research. 23 (12): 11864–11875.

Armendariz, A. L., M. A. Talano, C. Travaglia, H. Reinoso, A. L. Wevar Oller and E. Agostini, 2016. 'Arsenic toxicity in soybean seedlings and their attenuation mechanisms'. Plant Physiology and Biochemistry, 98: 119-127.

Banerjee, M., N. Banerjee, P. Bhattacharjee, D. Mondal, P. R. Lythgoe, M. Martínez, J. Pan, D. A. Polya and A. K. Giri, 2013. 'High arsenic in rice is associated with elevated genotoxic effects in humans'. Scientific Reports, 3: 2195-2203.

Bienert G. P. M. Thorsen, M. D. Schüssler, H. R. Nilsson, A. Wagner, M. J. Tamas, and T. P. Jahn, 2008. 'A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes'. BMC Biology, 10(6):26-32.

Carey, A. M., K. G. Scheckel, E. Lombi, M. Newville, Y. Choi, G. J. Norton, J. M. Charnock, J. Feldmann, A. H. Price and A. A. Meharg, 2010. 'Grain unloading of arsenic species in rice'. Plant Physiology, 152: 309-319.

Chen, P., K. Yan, H. Shao and S. Zhao, 2013. 'Physiological mechanisms for high salt tolerance in wild soybean (Glycine soja) from yellow river delta, China: photosynthesis, osmotic regulation, ion flux and antioxidant capacity'. Plos One, 8 (12): e83227.

Delavar, K., F. Ghanati, H, Zare-Maivan and M. Behmanesh, 2017. 'Effects of silicon on the growth of maize seedlings under normal, aluminum, and salinity stress conditions'. Journal of Plant Nutrition, 40 (10): 1475-1484.

Duan, G., T. Kamiya, S. Ishikawa, T. Arao and T. Fujiwara, 2012. 'Expressing ScACR3 in rice enhanced arsenite efflux and reduced arsenic accumulation in rice grains'. Plant Cell Physiology, 53(1):154-63.

Dubois, M., K. A. Gilles, J. K. Hamilton, P. A. Rebers, and F. Smith, 1956. 'Colorimetric method for determination of sugars and related substances'. Analytical Chemistry, 28(3): 350–356.

Fahad, S., S. Hussain, S. Saud, S. Hassan, B. S. Chauhan, F. Khan, M. Z. Ihsan, A. Ullah, C. Wu and A. A. Bajwa, 2016. 'Responses of rapid Visco analyzer profile and other rice grain qualities to exogenously applied plant growth regulators under high day and high night temperatures'. PLoS ONE, 11(7): e0159590.

Franks, P. J., 2013. 'Passive and active stomatal control: either or both?' New Phytologist, 198 (2): 325–327.

Grieve, C. M., and S. R. Grattan, 1983. 'Rapid assay for determination of water soluble quaternary ammonium compounds'. Plant Soil, 70(2): 303–307.

Gupta, P., and A. K. Bhatnagar, 2015. 'Spatial distribution of arsenic in different leaf tissues and its effect on structure and development of stomata and trichomes in mung bean, Vigna radiata (L.) Wilczek'. Environmental and Experimental Botany, 109: 12–22.

Iqbal, N., A. Masood, R. Nazar, S. Syeed and N. A. Khan, 2010. 'Photosynthesis growth and antioxidant metabolism in mustard (Brassica juncea L.) cultivars differing in cadmium tolerance'. Agricultural Sciences in China, 9: 519-527.

Kamachi, K., T. Yamaya, T. Mae and K. Ojima, 1991. 'A role for glutamine synthetase in the remobilization of leaf nitrogen during natural senescence in rice leaves'. Plant Physiology, 96: 411-417.

Kazan, K., 2015. 'Diverse roles of jasmonates and ethylene in abiotic stress tolerance'. Trends in Plant Science, 20: 219–229.

Khan, A. A., T. McNeilly and J. C. Collins, 2000. 'Accumulation of amino acids, proline, and carbohydrates in response to aluminum and manganese stress in maize'. Journal of Plant Nuttition, 23(9): 1303–1314.

Khan, M. A., M. R. Islam, G. M. Panaullah, J. M. Duxbury, M. Jahiruddin and R. H. Loeppert, 2009. 'Fate of irrigation-water arsenic in rice soils of Bangladesh'. Plant Soil, 322: 263-277.

Ma, J. F., N. Yamaji, N. Mitani, X. Y. Xu, Y. H. Su, S. P. McGrath and F. J. Zhao, 2008. 'Transporters of arsenite in rice and their role in arsenic accumulation in rice grain'. Proceedings of The National Academy of Sciences, 105: 9931-9935.

Marchiol, L., L. Leita, M. Martin, A. Peressotti, and G. Zerbi, 1996. 'Physiological responses of two soybean cultivars to cadmium'. Journal of Environmental Quality, 25(3): 562–566.

Meharg, A. A., and L. Jardine, 2003. 'Arsenite transport into paddy rice (Oryza sativa) roots'. New Phytologist, 157: 39-44.

Mishra, P., and R. S. Dubey, 2013. 'Excess nickel modulates activities of carbohydrate metabolizing enzymes and induces accumulation of sugars by upregulating acid invertase and sucrose synthase in rice seedlings'. Biometals, 26(1): 97–111.

Peleg, Z., and E. Blumwald, 2011. 'Hormone balance and abiotic stress tolerance in crop plants'. Current Opinion in Plant Biology, 14: 290–295

Rucinska-Sobkowiak, R., 2016. 'Water relations in plants subjected to heavy metal stresses'. Acta Physiologiae Plantarum, 38(11): 1–13.

Sade, D., N. Sade, O. Shriki, S. Lerner, A. Gebremedhin, A. Karavani, Y. Brotman, S. Osorio, A. R. Fernie, L. Willmitzer, H. Czosnek, and M. Moshelion, 2014. 'Water balance, hormone homeostasis, and sugar signaling are all involved in Tomato resistance to Tomato yellow leaf curl virus'. Plant Physiology, 165(4): 1684-1697.

Smedley, P. L., and D. G. Kinniburgh, 2013. Arsenic in groundwater and the environment. In: Selinus, O. (Ed.), Essentials of Medical Geology. Springer, pp. 279–310.

Spoel, S. H., and X. Dong, 2008. 'Making sense of hormone crosstalk during plant immune responses'. Cell Host & Microbe, 3: 348–351.

Srivastava, S., A. K. Srivastava, P. Suprasanna and S. F. D'Souza, 2011.' Quantitative real-time expression profiling of aquaporins-isoforms and growth response of Brassica juncea under arsenite stress'. Molecular Biology Reports, 40(4): 2879-86.

Srivastava, S., and Y. K. Sharma, 2013. 'Arsenic occurrence and accumulation in soil and water of eastern districts of Uttar Pradesh, India'. Environmental Monitoring and Assessment, 185: 4995-5002.

Su, Y. H., S. P. McGrath and F. J. Zhao, 2010. 'Rice is more efficient in arsenite uptake and translocation than wheat and barley'. Plant Soil, 328: 27-34.

Talano, M. A., R. B. Cejas, P. S. González and E. Agostini, 2013. 'Arsenic effect on the model crop symbiosis Bradyrhizobium-soybean'. Plant Physiology and Biochemistry, 63: 8–14.

Tayefeh, M., S. M. Sadeghi, S. A. Noorhosseini J. Bacenetti and C. A. Damalas, 2018. 'Environmental impact of rice production based on nitrogen fertilizer use'. Environmental Science and Pollution Research 25: 1-11.

Vassilev, A., F. Lidon, P. Scotti, M.. da Graca, and I. Yordanov, 2004. 'Cadmiuminduced changes in chloroplast lipids and photosystem activities in barley plants'. Biologia Plantarum, 48: 153–156.

Vezza, M. E., A. Llanes, C. Travaglia, E. Agostini and M. A. Talano, 2018. 'Arsenic stress effects on root water absorption in soybean plants: Physiological and morphological aspects'. Plant Physiology and Biochemistry. 123: 8-17.

Voleníkova, M., and I. Ticha, 2001. 'Insertion profiles in stomatal density and sizes in Nicotiana tabacum L. plantlets'. Biologia Plantarum, 44: 161–165.

Wan, X. M., M. Lei, T. B. Chen, J. X. Yang, H. T. Liu and Y. Chen, 2015.' Role of transpiration in arsenic accumulation of hyperaccumulator Pteris vittata L.' Environmental Science and Pollution Research, 22(21): 16631–16639.

Wilkinson, S., G. R. Kudoyarova, D. S. Veselov, T. N. Arkhipova and W. J. Davies, 2012. 'Plant hormone interactions: innovative targets for crop breeding and management.' Journal of Experimental Botany, 63: 3499–3509.

Williams, P. N., M. R. Islam, E. E. Adomako, A. Raab, S. A. Hossain, Y. G. Zhu, J. Feldmann and A. A. Meharg, 2006. 'Increase in rice grain arsenic for regions of Bangladesh irrigating paddies with elevated arsenic in ground waters'. Environmental Science & Technology, 40: 4903-4908.

Williams, P. N., A., Raab, J. Feldmann and A. A. Meharg, 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: 2178-2183.

Wu, G., Z. Zhou, P. Chen, X. Tang, H. Shao and H. Wang, 2014. 'Comparative ecophysiological study of salt stress for wild and cultivated soybean species from the Yellow River Delta, China'. The Scientific World Journal, 2014: 1–13.

Wu, Z., H. Ren, S. P. McGrath, P. Wu and F. J. Zhao, 2011.' Investigating the contribution of the phosphate transport pathway to arsenic accumulation in rice'. Plant Physiology, 157: 498-508.

Xu, X. Y., S. P. McGrath, A. A. Meharg and F. J. Zhao, 2008. 'Growing rice aerobically markedly decreases arsenic accumulation'. Environmental Science & Technology, 42: 5574-5579.

Yadav, S. K., 2010. 'Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants'. South African Journal of Botany, 76:167-179.

Yancey, P.H., 2005. 'Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses'. Journal of Experimental Biology, 208: 2819-2830.

Zhang, J., C. Y. Zhao, J. Liu, R. Song, Y. X. Du, J. Z. Li, H. Z. Sun, G. L. Duan and Q. Z. Zhao, 2016.' Influence of sulfur on transcription of genes involved in arsenic accumulation in rice grains'. Plant Molecular Biology Reporter, 34: 556-565.

Zhao, F. J., S. P. McGrath and A. A. Meharg, 2010. 'Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies'. Annual Review of Plant Biology, 61: 535–559.

Zhao, F. J., J. F. Ma, A. A. Meharg and S. P. McGrath, 2009. 'Arsenic uptake and metabolism in plants'. New Phytologist, 181: 777-794.

Zhou J., J. Wang, K. Shi, X. J. Xia, Y. H. Zhou and J. Q. Yu, 2012. 'Hydrogen peroxide is involved in the cold acclimation-induced chilling tolerance of tomato plants'. Plant Physiology and Biochemistry, 60: 141-149.