Abstract
A green house experiment was conducted to evaluate the efficacy of soil application of selenium (Se) in modulating metabolic changes in rice under arsenic (As) stress. Rice plants were grown over soil amended with sodium arsenate (25, 50 and 100 μM kg-1 soil) with or without sodium selenate @ 0.5 and 1 mg kg-1 soil in a complete randomized experimental design, and photosynthetic efficiency, nutrient uptake and nitrogen metabolism in rice leaves were estimated at tillering and grain filling stages. Se treatments significantly improved the toxic effects of As on plant height, leaf dry weight and grain yield. Arsenate treatment reduced uptake of Na, Mg, P, K, Ca, Mn, Fe and Zn and lowered chlorophyll, carotenoids and activities of enzymes of nitrogen metabolism (nitrate reductase, nitrite reductase, glutamine synthase and glutamate synthase) in rice leaves at both the stages in a dose-dependent fashion. Se application along with As improved photosynthesis, nutrient uptake and arsenate-induced effects on activities of enzymes of nitrogen metabolism with maximum impact shown by As50 + Se1 combination. Application of Se can modulate photosynthetic efficiency, nutrient uptake and alterations in nitrogen metabolism in rice Cv PR126 due to As stress that helped plants to adapt to excess As and resulted in improved plant growth.
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References
Ali A (2020) Nitrate assimilation pathway in higher plants: critical role in nitrogen signalling and utilization. Plant Sci Today 7:182–192. https://doi.org/10.14719/pst.2020.7.2.637
AL-Kazzaz AGM (2020) Morpho-physiological study on the effect of lead stress and selenium foliar application on growth of dill plant anethumgraveolens L. Plant Arch 20(1):1777–1782
Alyemeni MN, Ahanger MA, Wijaya L, Alam P, Bhardwaj R, Ahmad P (2018) Selenium mitigates cadmium-induced oxidative stress in tomato (Solanum lycopersicum L.) plants by modulating chlorophyll fluorescence, osmolyte accumulation, and antioxidant system. Protoplasma 255:459–469. https://doi.org/10.1007/s00709-017-1162-4
Anjum SA, Tanveer M, Hussain S, Ashraf U, Khan I, Wang L (2017) Alteration in growth, leaf gas exchange, and photosynthetic pigments of maize plants under combined cadmium and arsenic stress. Wat Air and Soil Poll 228(1):13. https://doi.org/10.1007/s11270-016-3187-2
Anonymous (2022) Packages of practices for crops of Punjab Kharif. Punjab Agricultural University, Ludhiana, pp 1–16
Auobi AS, Behtash F, Vafaee Y (2020) Selenium mitigates cadmium toxicity by preventing oxidative stress and enhancing photosynthesis and micronutrient availability on radish (Raphanus sativus L.) cv. Cherry Belle. Environ Sci Pollut Res 27(11):12476–12490. https://doi.org/10.1007/s11356-020-07751-2
Ayyaz A, Amir M, Umer S, Iqbal M, Bano H, Gul HS, Noor Y, Javed M, Athar HR, Zafar ZU, Farooq MA (2020) Melatonin induced changes in photosynthetic efficiency as probed by OJIP associated with improved chromium stress tolerance in canola (Brassica napus L.). Heliyon 6(7):e04364. https://doi.org/10.1016/j.heliyon.2020.e04364
Bakhat HF, Zia Z, Fahad S, Abbas S, Hammad HM, Shahzad AN, Abbas F, Alharby H, Shahid M (2017) Arsenic uptake, accumulation and toxicity in rice plants: possible remedies for its detoxification: a review. Environ Sci Pollut Res 24(10):9142–9158. https://doi.org/10.1007/s11356-017-8462-2
Balakhnina TI, Nadezhkina ES (2017) Effect of selenium on growth and antioxidant capacity of Triticum aestivum L. during development of lead-induced oxidative stress. Russ J Plant Physiol 64(2):215–223. https://doi.org/10.1134/S1021443717010022
Begum M, Mondal S (2019) Relative toxicity of arsenite and arsenate on early seedling growth and photosynthetic pigments of rice. Curr J Appl Sci Technol 33:1–5. https://doi.org/10.9734/cjast/2019/v33i430087
Bojórquez-Quintal E, Escalante-Magaña C, Echevarría-Machado I, Martínez-Estévez M (2017) Aluminum, a friend or foe of higher plants in acid soils. Front Plant Sci 8:1767. https://doi.org/10.3389/fpls.2017.01767
Bulen WA (1956) The isolation and characterization of glutamate dehydrogenase from corn leaves. Arch Biochem Biophys 62:178–183. https://doi.org/10.1016/0003-9861(56)90100-x
Camara AY, Wana Y, Yua Y, Wanga Q, Li H (2018) Effect of selenium on uptake and translocation of arsenic in rice seedlings (Oryza sativa L.). Ecotoxicol Environ Safe 148:869–875
Chattopadhyay A, Singh AP, Kasote D, Sen I, Regina A (2021) Effect of phosphorus application on arsenic species accumulation and co-deposition of polyphenols in rice grain: phyto and food safety evaluation. Plants 10(2):281. https://doi.org/10.3390/plants10020281
Chengming Z, Tanaka N, Dwiyanti MS, Shenton M, Maruyama H, Shinano T, Qingnan C, Jun X, Watanabe T (2022) Ionomic profiling of rice genotypes and identification of varieties with elemental covariation effects. Rice Sci 29(1):76–88. https://doi.org/10.1016/j.rsci.2021.12.007
Ding Y, Di X, Norton GJ, Beesley L, Yin X, Zhang Z, Zhi S (2020) Selenite foliar application alleviates arsenic uptake, accumulation, migration and increases photosynthesis of different upland rice varieties. Int J Environ Res Public Health 17(10):3621. https://doi.org/10.3390/ijerph17103621
Dogra V, Duan J, Lee KP, Kim C (2019) Impaired PSII proteostasis triggers a UPR-like response in the var2 mutant of Arabidopsis. J Exp Bot 70(12):3075–3088. https://doi.org/10.1093/jxb/erz151
Dwivedi S, Kumar A, Mishra S, Sharma P, Sinam G, Bahadur L, Tripathi RD (2020) Orthosilicic acid (OSA) reduced grain arsenic accumulation and enhanced yield by modulating the level of trace element, antioxidants, and thiols in rice. Environ Sci Pollut Res 27:24025–24038. https://doi.org/10.1007/s11356-020-08663-x
Feng R, Zhao P, Zhu Y, Yang J, Wei X, Yang L, Liu H, Rensing C, Ding Y (2021) Application of inorganic selenium to reduce accumulation and toxicity of heavy metals (metalloids) in plants: the main mechanisms, concerns, and risks. Sci Total Environ 771:144776. https://doi.org/10.1016/j.scitotenv.2020.144776
Ferari TE, Verner JE (1971) Intact tissue assay for nitrate reductase in barley aleuton layers. Plant Physiol 47:790–794. https://doi.org/10.1104/pp.47.6.790
Gao J, Wang H, Yuan Q, Feng Y (2018) Structure and function of the photosystem supercomplexes. Front Plant Sci 9:357. https://doi.org/10.3389/fpls.2018.00357
Ghosh S, Biswas AK (2017) Selenium modulates growth and thiol metabolism in wheat (Triticum aestivum L.) during arsenic stress. Am J Plant Sci 8:363. https://doi.org/10.4236/ajps.2017.83026
Hassanein YZ, Abdel-Rahman SSA, Soliman WS, Salaheldin S (2021) Growth, yield, and quality of roselle (Hibiscus sabdariffa L.) plants as affected by nano zinc and bio-stimulant treatments. Horti Environ Biotechnol 62(6):879–890. https://doi.org/10.1007/s13580-021-00371-w
Hossain MM, Khatu MA, Haque MN, Bari MA, Alam MF, Mandal A, Kabir AH (2018) Silicon alleviates arsenic-induced toxicity in wheat through vacuolar sequestration and ROS scavenging. Int J Phytoremediation 20(8):796–804. https://doi.org/10.1080/15226514.2018.1425669
Hussain B, Lin Q, Hamid Y, Sanaullah M, Di L, Khan MB, He Z, Yang X (2020a) Foliage application of selenium and silicon nanoparticles alleviates Cd and Pb toxicity in rice (Oryza sativa L.). Sci Total Environ 712-136497https://doi.org/10.1016/j.scitotenv.2020a.136497
Hussain I, Saleem MH, Mumtaz S, Rasheed R, Ashraf MA, Maqsood F, Rehman M, Yasmin H, Ahmed S, Ishtiaq M, Anwar S (2021) Choline chloride mediates chromium tolerance in spinach (spinacia oleracea l.) by restricting its uptake in relation to morpho-physio-biochemical attributes. J Plant Growth Reg 1–21. https://doi.org/10.1007/s00344-021-10401-7
Hussain S, Khaliq A, Noor MA, Tanveer M, Hussain HA, Hussain S, Shah T, Mehmood T (2020b) Metal toxicity and nitrogen metabolism in plants: an overview. In: Datta R, Meena RS, Pathan SI, Ceccherini MT (eds) Carbon and nitrogen cycling in soil. Springer, Singapore, pp 221–248. https://doi.org/10.1007/978-981-13-7264-3_7
Jowarski E (1971) Nitrate reductase assay in intact plant tissues. Biochem Biophys Res Commun 48:1274–1279. https://doi.org/10.1016/S0006-291X(71)80010-4
Kalita J, Pradhan AK, Shandilya ZM, Tanti B (2018) Arsenic stress responses and tolerance in rice: physiological, cellular and molecular approaches. Rice Sci 25:235–249. https://doi.org/10.1016/j.rsci.2018.06.007
Kanamori T, Matsumoto H (1974) Asparagine synthesis by Oryza sativa seedlings. Phytochem 13:1407–1412. https://doi.org/10.1016/0031-9422(74)80300-6
Karimi R, Ghabooli M, Rahimi J, Amerian M (2020) Effects of foliar selenium application on some physiological and phytochemical parameters of Vitisvinifera L cv Sultana under salt stress. J Plant Nutr 43(14):2226–42. https://doi.org/10.1080/01904167.2020.1766072
Kaur M, Sharma S (2018) Influence of selenite and selenate on growth, leaf physiology and antioxidant defense system in wheat (Triticumaestivum L.). J Sci Food Agric 98(15):5700–5710. https://doi.org/10.1002/jsfa.9117
Kaur S, Singh D, Singh K (2017) Effect of selenium application on arsenic uptake in rice (Oryza sativa L.). Environ Monit Assess 189:430. https://doi.org/10.1007/s10661-017-6138-5
Kaya C, Sarioglu A, Ashraf M, Alyemeni MN, Ahmad P (2022) The combined supplementation of melatonin and salicyclic acid effectively detoxifies arsenic toxicity by modulating phytochelatins and nitrogen metabolism in pepper plants. Environ Pollut 297:118727. https://doi.org/10.1016/j.envpol.2021.118727
Khalid S, Shahid M, Niazi NK, Rafiq M, Bakhat HF, Imran M, Abbas T, Bibi I, Dumat C (2017) Arsenic behaviour in soil-plant system: biogeochemical reactions and chemical speciation influences. In: Enhancing cleanup of environmental pollutants. Anjum, NA; Gill, SS; Tuteja, N Editors. (pp. 97–140): Springer. https://doi.org/10.1007/978-3-319-55423-5_4
Kocheva K, Kartseva T, Nenova V, Georgiev G, Brestič M, Misheva S (2020) Nitrogen assimilation and photosynthetic capacity of wheat genotypes under optimal and deficient nitrogen supply. Physiol Mol Biol Plants 26(11):2139–2149. https://doi.org/10.1007/s12298-020-00901-3
Kojima S, Ishiyama K, Beier MP, Hayakawa T (2020) Ammonium assimilation and metabolism in rice. In Progress in botany Vol. 82 (pp. 211–231). Springer, Cham
Kumar A, Dixit G, Singh AP, Dwivedi S, Srivastava S, Mishra K, Tripathi RD (2016) Selenate mitigates arsenite toxicity in rice (Oryza sativa L.) by reducing arsenic uptake and ameliorates amino acid content and thiol metabolism. Ecotoxicol Environ Saf 133:350–359. https://doi.org/10.1016/j.ecoenv.2016.06.037
Li X, Ma L, Li Y, Wang L, Zhang L (2019) Endophyte infection enhances accumulation of organic acids and minerals in rice under Pb2+ stress conditions. Ecotoxicol Environ Saf 174:255–262. https://doi.org/10.1016/j.ecoenv.2019.02.072
Majumder B, Das S, Biswas S, Mazumdar A, Biswas AK (2020) Differential responses of photosynthetic parameters and its influence on carbohydrate metabolism in some contrasting rice (Oryza sativa L.) genotypes under arsenate stress. Ecotoxicology 29:912–931. https://doi.org/10.1007/s10646-020-02241-0
Majumder B, Das S, Mukhopadhyay S, Biswas AK (2019) Identification of arsenic-tolerant and arsenic-sensitive rice (Oryza sativa L.) cultivars on the basis of arsenic accumulation assisted stress perception, morpho-biochemical responses, and alteration in genomic template stability. Protoplasma 256(1):193–211. https://doi.org/10.1007/s00709-018-1290-5
Maslova TG, Markovskaya EF, Slemnev NN (2021) Functions of carotenoids in leaves of higher plants. Biol Bull Rev 11(5):476–487. https://doi.org/10.1134/S2079086421050078
Mroczek-Zdyrska M, Strubińska J, Hanaka A (2017) Selenium improves physiological parameters and alleviates oxidative stress in shoots of lead-exposed Viciafaba L. minor plants grown under phosphorus-deficient conditions. J Plant Growth Regul 36(1):186–199. https://doi.org/10.1007/s00344-016-9629-7
Murugaiyan V, Zeibig F, Anumalla M, Siddiq SA, Frei M, Murugaiyan J, Ali J (2021) Arsenic stress responses and accumulation in rice. Rice Improv 281-313.https://doi.org/10.1007/978-3-030-66530-2_9
Nicol L, Nawrocki WJ, Croce R (2019) Disentangling the sites of non-photochemical quenching in vascular plants. Nat Plants 5(11):1177–1183. https://doi.org/10.1038/s41477-019-0526-5
Pandey C, Gupta M (2018) Selenium amelioration of arsenic toxicity in rice shows genotypic variation: a transcriptomic and biochemical analysis. J Plant Physiol 231:168–181. https://doi.org/10.1016/j.jplph.2018.09.013
Pita-Barbosa A, Williams TCR, Loureiro ME (2019) Effects of short-term arsenic exposure in Arabidopsis thaliana: tolerance versus toxicity responses. Biol Plant 63:43–53. https://doi.org/10.32615/bp.2019.006
Sali A, Zeka D, Fetahu S, Rusinovci I, Kaul AP (2018) Selenium supply affects chlorophyll concentration and biomass production of maize (Zea mays L.). Bodenkultur J Land Manag Food Environ 69:249–255. https://doi.org/10.2478/boku-2018-0021
Sandil S, Dobosy P, Kröpfl K, Füzy A, Óvári M, Záray G (2019) Effect of irrigation water containing arsenic on elemental composition of bean and lettuce plants cultivated in calcareous sandy soil. Food Prod Process and Nutr 1(1):1–10. https://doi.org/10.1186/s43014-019-0014-3
Sharma S, Sharma A, Singh D (2018) Effect of sodium selenate on photosynthetic efficiency, antioxidative defence system and micronutrients in maize. Biologia 73(2):137–144
Siddiqui MH, Alamri S, Khan MN, Corpas FJ, Al-Amri AA, Alsubaie QD, Ali HM, Kalaji HM, Ahmad P (2020) Melatonin and calcium function synergistically to promote the resilience through ROS metabolism under arsenic induced stress. J Hazard Mater 398:122882. https://doi.org/10.1016/j.jhazmat.2020.122882
Sil P, Das P, Biswas AK (2018) Silicon induced mitigation of TCA cycle and GABA synthesis in arsenic stressed wheat (Triticumaestivum L.) seedlings. S Afr J Bot 119:340–352. https://doi.org/10.1016/j.sajb.2018.09.035
Sil P, Das P, Biswas AK (2019a) Impact of exogenous silicate amendments on nitrogen metabolism in wheat seedlings subjected to arsenate stress. SILICON 12:535–545. https://doi.org/10.1007/s12633-019-00158-w
Sil P, Das P, Biswas S, Mazumdar A, Biswas AK (2019) Modulation of photosynthetic parameters, sugar metabolism, polyamine and ion contents by silicon amendments in wheat (Triticum aestivum L) seedlings exposed to arsenic. Environ Sci Pollut Res 26(13):13630–13648. https://doi.org/10.1007/s11356-019-04896-7
Singh R, Upadhyay A, Singh K (2018) Regulation of oxidative stress and mineral nutrient status by selenium in arsenic treated crop plant Oryza sativa. Ecotoxicol Environ Saf 148:105–113. https://doi.org/10.1016/j.ecoenv.2017.10.008
Suriyagoda LDB, Dittert K, Lambers H (2018) Mechanism of arsenic uptake, translocation and plant resistance to accumulate arsenic in rice grains. Agric Ecosust Environ 253:23–37. https://doi.org/10.1016/j.agee.2017.10.017
Ulhassan Z, Huang Q, Gill RA, Ali S, Mwamba TM, Ali B, Hina F, Zhou W (2019) Protective mechanisms of melatonin against selenium toxicity in Brassica napus: insights into physiological traits, thiol biosynthesis and antioxidant machinery. BMC Plant Biol 19(1):1–16. https://doi.org/10.1186/s12870-019-2110-6
Uppal JS, Zheng Q, Le XC (2019) Arsenic in drinking water—recent examples and updates from Southeast Asia. Curr Opin Environ Sci Health 7:126–135. https://doi.org/10.1016/j.coesh.2019.01.004
Wang K, Wang Y, Wan Y, Mi Z, Wang Q, Wang Q, Li H (2021) The fate of arsenic in rice plants: influence of different forms of selenium. Chemosphere 264:128417. https://doi.org/10.1016/j.chemosphere.2020.128417
Wang P, Chen X, Xu X, Lu C, Zhang W, Zhao FJ (2018) Arsenate induced chlorosis 1/translocon at the outer envelope membrane of chloroplasts 132 protects chloroplasts from arsenic toxicity. Plant Physiol 178:1568–1583. https://doi.org/10.1104/pp.18.01042
Wany A, Pathak PK, Gupta KJ (2020) Methods for measuring nitrate reductase, nitrite levels, and nitric oxide from plant tissues. In Nitrogen metabolism in plants (pp. 15–26). Humana, New York, NY (2020). https://doi.org/10.1007/978-1-4939-9790-9_2
Wellburn AR, Lichtenthaler H (1984) Formulae and program to determine total carotenoids and chlorophylls a and b of leaf extracts in different solvents. In Advances in photosynthesis research, (pp. 9–12). Springer, Dordrecht
Xia Q, Yang Z, Shui Y, Liu X, Chen J, Khan S, Wang J, Gao Z (2020) Methods of selenium application differentially modulate plant growth, selenium accumulation and speciation, protein, anthocyanins and concentrations of mineral elements in purple-grained wheat. Front Plant Sci 11:1114. https://doi.org/10.3389/fpls.2020.01114
Zemanová V, Popov M, Pavlíková D, Kotrba P, Hnilička F, Česká J, Pavlík M (2020) Effect of arsenic stress on 5-methylcytosine, photosynthetic parameters and nutrient content in arsenic hyperaccumulator Pteriscretica (L.) var. Albo-lineata. BMC Plant Biol 20(1):1–10
Zeng H, Zhang X, Ding M, Zhang X, Zhu Y (2019) Transcriptome profiles of soybean leaves and roots in response to zinc deficiency. Physiol Plant 167:330–351. https://doi.org/10.1111/ppl.12894
Zhao Y, Hu C, Wang X, Qin X, Wang P, Zhang Y, Zhang X, Zhao X (2019) Selenium alleviated chromium stress in Chinese cabbage (Brassica campestris L. ssp.Pekinensis) by regulating root morphology and metal element uptake. Ecotox Environ Safe 173:314–321. https://doi.org/10.1016/j.ecoenv.2019.01.090
Zhou XB, Gao AX, Lai F, Zhang CM, Xu WH (2017) The role of selenium in soil: effect on the uptake and translocation of arsenic in rice. Int J Agric Biol 19:1227–1234. https://doi.org/10.17957/IJAB/15.0430
Zvobgo G, LwalabaWaLwalaba J, Sagonda T, Mapodzeke JM, Muhammad N, Shamsi IH, Zhang G (2018) Phosphate alleviates arsenate toxicity by altering expression of phosphate transporters in the tolerant barley genotypes. Ecotoxicol Environ Saf 147:832–839. https://doi.org/10.1016/j.ecoenv.2017.09.043
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The authors are thankful to Dr Dhanwinder Singh, principal soil chemist, for his help in sowing of crop.
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We acknowledge funding support from University Grant Commission, New Delhi for providing senior research fellowship to SB.
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SS: conceived and designed the experiments, analyzed the data and finalized manuscript; SB: performed the experiments, compilation of data, prepared rough draft. Both the authors have read the final manuscript and approved the submission.
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Bhadwal, S., Sharma, S. Selenium alleviates physiological traits, nutrient uptake and nitrogen metabolism in rice under arsenate stress. Environ Sci Pollut Res 29, 70862–70881 (2022). https://doi.org/10.1007/s11356-022-20762-5
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DOI: https://doi.org/10.1007/s11356-022-20762-5