Effects of Selenium on DNA Methylation and Genomic Instability Induced by Drought Stress in Wheat (Triticum aestivum L.)

Yıl 2024, , 26 - 37, 03.04.2024

Zehra Şahin , Güleray Ağar , Esma Yiğider , Murat Aydın

https://doi.org/10.19159/tutad.1380744

Cited By: 1

Öz

The main purpose of the study was to clarify the effect of selenium (Se) on DNA damage and DNA methylation in wheat (Triticum aestivum L.) plants exposed to polyethylene glycol (PEG)-induced drought stress under in vitro tissue culture. Random amplified polymorphic DNA (RAPD) and coupled restriction enzyme digestion-random amplification (CRED-RA) were utilized to explain the DNA damage grade and variations in DNA methylation patterns, respectively. The outcomes indicate that drought stress gives rise to a rise in RAPD profile variations (as DNA damage) and a decrease in genomic template stability (GTS) rate and DNA methylation changes. According to the RAPD data, the greatest GTS value was computed at 56.9% (5% PEG 6000), and the lowest GTS value was 41.2% (15% PEG 6000), demonstrating the adverse effects of PEG 6000. However, DNA damage can be reduced by treatment with sodium selenate (2, 4, and 6 µM of Na2SeO4) together with PEG (5%, 10%, and 15% PEG 6000)-induced water deficits. Moreover, according to CRED-RA analysis, PEG-induced DNA methylation rates were changed after treating different doses of Se. These data demonstrate that Se dose-dependently modulates both DNA damage and methylation alterations induced by drought in wheat.

Anahtar Kelimeler

DNA damage, DNA methylation, drought stress, polyethylene glycol, selenium

Kaynakça

• Andrade, F.R., da Silva, G.N., Guimarães, K.C., Barreto, H.B.F., de Souza, K.R.D., Guilherme, L.R.G., Faquin, V., dos Reis, A.R., 2018. Selenium protects rice plants from water deficit stress. Ecotoxicology and Environmental Safety, 164: 562-570.
• Ashapkin, V.V., Kutueva, L.I., Aleksandrushkina, N.I., Vanyushin, B.F., 2020. Epigenetic mechanisms of plant adaptation to biotic and abiotic stresses. International journal of molecular sciences, 21(20): 7457.
• Awan, S.A., Khan, I., Rizwan, M., Zhang, X., Brestic, M., Khan, A., El-Sheikh, M.A., Alyemeni, M.N., Ali, S., Huang, L., 2021. Exogenous abscisic acid and jasmonic acid restrain polyethylene glycol‐induced drought by improving the growth and antioxidative enzyme activities in pearl millet. Physiologia Plantarum, 172(2): 809-819.
• Aydin, M., Taşpınar, M.S., Arslan, E., Yağci, S., Ağar, G., 2017. Dicamba causes genomic instability in Phaseolus vulgaris seedlings. II. International Conference on Advances in Natural and Applied Sciences, AIP Conference Proceedings, April 18-21, Antalya, Turkey, pp. 020063.
• Banerjee, A., Roychoudhury, A., 2017. Epigenetic regulation during salinity and drought stress in plants: histone modifications and DNA methylation. Plant Gene, 11: 199-204.
• Begna, T., 2020. Effects of drought stress on crop production and productivity. International Journal of Research Studies in Agricultural Sciences, 6: 34-43.
• Bhat, A.H., Dar, K.B., Anees, S., Zargar, M.A., Masood, A., Sofi, M.A., Ganie, S.A., 2015. Oxidative stress, mitochondrial dysfunction, and neurodegenerative diseases; a mechanistic insight. Biomedicine & Pharmacotherapy, 74: 101-110.
• Bocchini, M., D’Amato, R., Ciancaleoni, S., Fontanella, M.C., Palmerini, C.A., Beone, G.M., Onofri, A., Negri, V., Marconi, G., Albertini, E., 2018. Soil selenium (Se) biofortification changes the physiological, biochemical, and epigenetic responses to water stress in Zea mays L. by inducing a higher drought tolerance. Frontiers in Plant Science, 9: 389.
• Cartes, P., Jara, A., Pinilla, L., Rosas, A., Mora, M., 2010. Selenium improves the antioxidant ability against aluminium‐induced oxidative stress in ryegrass roots. Annals of Applied Biology, 156(2): 297-307.
• Cho, D., Shin, D., Jeon, B.W., Kwak, J.M., 2009. ROS-mediated ABA signaling. Journal of Plant Biology, 52(2): 102-113.
• Chu, J., Yao, X., Zhang, Z., 2010. Responses of wheat seedlings to exogenous selenium supply under cold stress. Biological Trace Element Research, 136(3): 355-363.
• Creppy, E.E., Traoré, A., Baudrimont, I., Cascante, M., Carratú, M.R., 2002. Recent advances in the study of epigenetic effects induced by the phycotoxin okadaic acid. Toxicology, 181: 433-439.
• de Oliveira, A.B., Alencar, N. L. M., Gomes-Filho, E., 2013. Comparison between the water and salt stress effects on plant growth and development. In: S. Akıncı (Ed.), Responses of Organisms to Water Stress, IntechOpen Limited, United Kingdom, 4: 67-94.
• de Sousa, G.F., Silva, M.A., de Morais, E.G., Van Opbergen, G.A.Z., Van Opbergen, G.G.A., de Oliveira, R.R., Amaral, D., Brown, P., Chalfun-Junior, A., Guilherme, L.R.G., 2022. Selenium enhances chilling stress tolerance in coffee species by modulating nutrient, carbohydrates, and amino acids content. Frontiers in Plant Science, 13: 3259.
• Dhar, M.K., Sharma, R., Vishal, P., Kaul, S., 2019. Epigenetic response of plants to abiotic stress: Nature, consequences and applications in breeding. In: V. Rajpal, D. Sehgal, A. Kumar and S. Raina (Eds.), Genetic Enhancement of Crops for Tolerance to Abiotic Stress: Mechanisms and Approaches, Springer, Switzerland, Vol. I, pp. 53-72.
• Djanaguiraman, M., Devi, D.D., Shanker, A.K., Sheeba, J.A., Bangarusamy, U., 2005. Selenium–an antioxidative protectant in soybean during senescence. Plant and Soil, 272(1-2): 77-86.
• Erturk, F.A., Agar, G., Arslan, E., Nardemir, G., Aydin, M., Taspinar, M.S., 2014. Effects of lead sulfate on genetic and epigenetic changes, and endogenous hormone levels in corn (Zea mays L.). Polish Journal of Environmental Studies, 23(6): 1925-1932.
• Fahad, S., Hussain, S., Saud, S., Khan, F., Hassan, S., Nasim, W., Arif, M., Wang, F., Huang, J., 2016. Exogenously applied plant growth regulators affect heat‐stressed rice pollens. Journal of Agronomy and Crop Science, 202(2): 139-150.
• Filek, M., Keskinen, R., Hartikainen, H., Szarejko, I., Janiak, A., Miszalski, Z., Golda, A., 2008. The protective role of selenium in rape seedlings subjected to cadmium stress. Journal of Plant Physiology, 165(8): 833-844.
• Ge, C., Yang, X., Liu, X., Sun, H., Luo, S., Wang, Z., 2012. Effect of heavy metal on levels of methylation in DNA of rice and wheat. Journal of Plant Physiology and Molecular Biology, 28(5): 363-368.
• Genchi, G., Lauria, G., Catalano, A., Sinicropi, M.S., Carocci, A., 2023. Biological activity of selenium and its impact on human health. International Journal of Molecular Sciences, 24(3): 2633.
• Geng, A., Lian, W., Wang, Y., Liu, M., Zhang, Y., Wang, X., Chen, G., 2024. Molecular mechanisms and regulatory pathways underlying drought stress response in rice. International Journal of Molecular Sciences, 25(2): 1185.
• Golob, A., Kugovnik, A., Kreft, I., Gaberščik, A., Germ, M., 2019. The interactions between UV radiation, drought and selenium in different buckwheat species. Acta Biologica Slovenica, 62(1): 57-66.
• Grativol, C., Hemerly, A.S., Ferreira, P.C.G., 2012. Genetic and epigenetic regulation of stress responses in natural plant populations. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms, 1819(2): 176-185.
• Gupta, A.K., Agrawal, M., Yadav, H., Mishra, G., Gupta, R., Singh, A., Katiyar, D., Singh, P., Srivastava, A., 2024. Drought stress and its tolerance mechanism in wheat. International Journal of Environment and Climate Change, 14(1): 529-544.
• Gupta, M., Gupta, S., 2017. An overview of selenium uptake, metabolism, and toxicity in plants. Frontiers in Plant Science, 7: 2074.
• Hartikainen, H., 2005. Biogeochemistry of selenium and its impact on food chain quality and human health. Journal of Trace Elements in Medicine and Biology, 18(4): 309-318.
• Hasanuzzaman, M., Hossain, M.A., Fujita, M., 2012. Exogenous selenium pretreatment protects rapeseed seedlings from cadmium-induced oxidative stress by upregulating antioxidant defense and methylglyoxal detoxification systems. Biological Trace Element Research, 149(2): 248-261.
• Huang, Z., Meng, S., Huang, J., Zhou, W., Song, X., Hao, P., Tang, P., Cao Y., Zhang, F., Li, H., Tang, Y., Sun, B., 2024. Transcriptome analysis reveals the mechanism of exogenous selenium in alleviating cadmium stress in purple flowering stalks (Brassica campestris var. purpuraria). International Journal of Molecular Sciences, 25(3): 1800.
• Jaskulak, M., Grobelak, A., Grosser, A., Vandenbulcke, F., 2019. Gene expression, DNA damage and other stress markers in Sinapis alba L. exposed to heavy metals with special reference to sewage sludge application on contaminated sites. Ecotoxicology and Environmental Safety, 181: 508-517.
• Jiang, C., Zu, C., Lu, D., Zheng, Q., Shen, J., Wang, H., Li, D., 2017. Effect of exogenous selenium supply on photosynthesis, Na+ accumulation and antioxidative capacity of maize (Zea mays L.) under salinity stress. Scientific Reports, 7: 42039.
• Jiang, J., Chen, B., Tang, B., Wei, Q., 2023. Selenium in prostate cancer: Prevention, progression, and treatment. Pharmaceuticals, 16(9): 1250.
• Kawai, K., Kasai, H., Li, Y.S., Kawasaki, Y., Watanabe, S., Ohta, M., Honda, T., Yamato, H., 2018. Measurement of 8-hydroxyguanine as an oxidative stress biomarker in saliva by HPLC-ECD. Genes and Environment, 40(1): 5.
• Kong, L., Wang, M., Bi, D., 2005. Selenium modulates the activities of antioxidant enzymes, osmotic homeostasis and promotes the growth of sorrel seedlings under salt stress. Plant Growth Regulation, 45(2): 155-163.
• Kumar, M., Bijo, A., Baghel, R.S., Reddy, C., Jha, B., 2012. Selenium and spermine alleviate cadmium induced toxicity in the red seaweed Gracilaria dura by regulating antioxidants and DNA methylation. Plant Physiology and Biochemistry, 51: 129-138.
• Kumar, A., Singh, R.P., Singh, P.K., Awasthi, S., Chakrabarty, D., Trivedi, P.K., Tripathi, R.D., 2014. Selenium ameliorates arsenic induced oxidative stress through modulation of antioxidant enzymes and thiols in rice (Oryza sativa L.). Ecotoxicology, 23(7): 1153-1163.
• Kuznetsov, V.V., Radyukina, N.L., Shevyakova, N.I., 2006. Polyamines and stress: Biological role, metabolism, and regulation. Russian Journal of Plant Physiology, 53(5): 583-604.
• Lämke, J., Bäurle, I., 2017. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biology, 18(1): 124.
• Li, M., Chen, W-D., Papadopoulos, N., Goodman, S.N., Bjerregaard, N.C., Laurberg, S., Levin, B., Juhl, H., Arber, N., Moinova, H., 2009. Sensitive digital quantification of DNA methylation in clinical samples. Nature Biotechnology, 27(9): 858.
• Liu, K., Zhao, Y., Chen, F., Gu, Z., Bu, G., 2011. Enhanced glutathione peroxidases (GPx) activity in young barley seedlings enriched with selenium. African Journal of Biotechnology, 10(55): 11482-11487.
• Lu, L., Katsaros, D., de la Longrais, I.A.R., Sochirca, O., Yu, H., 2007. Hypermethylation of let-7a-3 in epithelial ovarian cancer is associated with low insulin-like growth factor-II expression and favorable prognosis. Cancer Research, 67(21): 10117-10122.
• Marnett, L.J., Riggins, J.N., West, J.D., 2003. Endogenous generation of reactive oxidants and electrophiles and their reactions with DNA and protein. The Journal of Clinical Investigation, 111(5): 583-593.
• Martinez, V., Nieves-Cordones., M., Lopez-Delacalle, M., Rodenas, R., Mestre, T., Garcia-Sanchez, F., Rubio, F., Nortes, P., Mittler, R., Rivero, R., 2018. Tolerance to stress combination in tomato plants: New insights in the protective role of melatonin. Molecules, 23(3): 535.
• Murashige, T., Skoog, F., 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum, 15(3): 473-497.
• Nawaz, F., Naeem, M., Ashraf, M.Y., Tahir, M.N., Zulfiqar, B., Salahuddin, M., Shabbir, R.N., Aslam, M., 2016. Selenium supplementation affects physiological and biochemical processes to improve fodder yield and quality of maize (Zea mays L.) under water deficit conditions. Frontiers in Plant Science, 7: 1438.
• Öztürk, A., Bayram, S., Haliloğlu, K., Aydın, M., Çağlar, Ö., Bulut, S., 2014. Characterization for drought resistance at early stages of wheat genotypes based on survival, coleoptile length, and seedling vigor. Turkish Journal of Agriculture and Forestry, 38(6): 824-837.
• Pandey, J., Devadasu, E., Saini, D., Dhokne, K., Marriboina, S., Raghavendra, A.S., Subramanyam, R., 2023. Reversible changes in structure and function of photosynthetic apparatus of pea (Pisum sativum) leaves under drought stress. The Plant Journal, 113(1): 60-74.
• Pennanen, A., Tailin, X., Hartikainen, H., 2002. Protective role of selenium in plant subjected to severe UV irradiation stress. Journal of Applied Botany, 76(1-2): 66-76.
• Pérez-Clemente, R.M., Gómez-Cadenas, A., 2012. In vitro tissue culture, a tool for the study and breeding of plants subjected to abiotic stress conditions. In: A. Leva and L.M.R. Rinaldi (Eds.), Recent Advances in Plant In Vitro Culture, IntechOpen Limited, United Kingdom, pp. 91-108.
• Pikaard, C.S., Scheid, O.M., 2014. Epigenetic regulation in plants. Cold Spring Harbor Perspectives in Biology, 6(12): a019315.
• Proietti, P., Nasini, L., Del Buono, D., D’Amato, R., Tedeschini, E., Businelli, D., 2013. Selenium protects olive (Olea europaea L.) from drought stress. Scientia Horticulturae, 164: 165-171.
• Rao, S., Ftz, J., 2013. In vitro selection and characterization of polyethylene glycol (PEG) tolerant callus lines and regeneration of plantlets from the selected callus lines in sugarcane (Saccharum officinarum L.). Physiology and Molecular Biology of Plants, 19(2): 261-268.
• Rasool, A., Hafiz Shah, W., Padder, S.A., Tahir, I., Alharby, H.F., Hakeem, K.R., ul Rehman, R., 2023. Exogenous selenium treatment alleviates salinity stress in proso millet (Panicum miliaceum L.) by enhancing the antioxidant defence system and regulation of ionic channels. Plant Growth Regulation, 100(2): 479-494.
• Raza, M.A.S., Aslam, M.U., Valipour, M., Iqbal, R., Haider, I., Mustafa, A.E.Z.M., Elshikh M.S., Ali, I., Roy, R., Elshamly, A.M., 2024. Seed priming with selenium improves growth and yield of quinoa plants suffering drought. Scientific Reports, 14(1): 886.
• Reis, A.R., Favarin, J.L., Gratão, P.L., Capaldi, F.R., Azevedo, R.A., 2015. Antioxidant metabolism in coffee (Coffea arabica L.) plants in response to nitrogen supply. Theoretical and Experimental Plant Physiology, 27(3-4): 203-213.
• Sahu, M., Maurya, S., Jha, Z., 2023. In vitro selection for drought and salt stress tolerance in rice: An overview. Plant Physiology Reports, 28(1): 8-33.
• Sahu, P.P., Pandey, G., Sharma, N., Puranik, S., Muthamilarasan, M., Prasad, M., 2013. Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Reports, 32(8): 1151-1159.
• Sallam, N., Moussa, M., Yacout, M., El-Seedy, A., 2019. Differential DNA methylation under drought stress in maize. International Journal of Current Microbiology and Applied Sciences, 8(8): 2527-2543.
• Schwarz, K., Foltz, C.M., 1957. Selenium as an integral part of factor 3 against dietary necrotic liver degeneration. Journal of the American Chemical Society, 79(12): 3292-3293.
• Sharma, I., Tyagi, B.S., Singh, G., Venkatesh, K., Gupta, O.P., 2015. Enhancing wheat production-A global perspective. Indian Journal of Agricultural Sciences, 85(1): 3-13.
• Shim, J.S., Oh, N., Chung, P.J., Kim, Y.S., Choi, Y.D., Kim, J.K., 2018. Overexpression of OsNAC14 improves drought tolerance in rice. Frontiers in Plant Science, 9: 310.
• Si, Y., Zhang, C., Meng, S., Dane, F., 2009. Gene expression changes in response to drought stress in Citrullus colocynthis. Plant Cell Reports, 28(6): 997-1009.
• Song, J., Xin, L., Gao, F., Liu, H., Wang, X., 2024. Effects of foliar selenium application on oxidative damage and photosynthetic properties of greenhouse tomato under drought stress. Plants, 13(2): 302.
• Tabassum, N., Sony, S.K., Bhajan, S.K., Islam, M.N., 2013. Analysis of genetic diversity in eleven tomato (Lycopersicon esculentum Mill.) varieties using RAPD markers. Plant Tissue Culture and Biotechnology, 23(1): 49-57.
• Tan, M.P., 2010. Analysis of DNA methylation of maize in response to osmotic and salt stress based on methylation-sensitive amplified polymorphism. Plant Physiology and Biochemistry, 48(1): 21-26.
• Taspinar, M.S., Agar, G., Yildirim, N., Sunar, S., Aksakal, O., Bozari, S., 2009. Evaluation of selenium effect on cadmium genotoxicity in Vicia faba using RAPD. Journal of Food, Agriculture and Environment, 7(4): 857-860.
• Turhan, S., Taspinar, M.S., Yigider, E., Aydin, M., Agar, G., 2021. The role of long terminal repeat (LTR) responses to drought in selenium-treated wheat. Environmental Engineering & Management Journal, 20(6): 917-925.
• Valinluck, V., Tsai, H.H., Rogstad, D.K., Burdzy, A., Bird, A., Sowers, L.C., 2004. Oxidative damage to methyl-CpG sequences inhibits the binding of the methylCpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Research, 32(14): 4100-4108.
• Yanagi, M., 2024. Climate change impacts on wheat production: Reviewing challenges and adaptation strategies. Advances in Resources Research, 4(1): 89-107.
• Yao, X., Chu, J., Liang, L., Geng, W., Li, J., Hou, G., 2012. Selenium improves recovery of wheat seedlings at rewatering after drought stress. Russian Journal of Plant Physiology, 59(6): 701-707.
• Yao, X., Chu, J., Wang, G., 2009. Effects of selenium on wheat seedlings under drought stress. Biological Trace Element Research, 130(3): 283-290.
• Zhang, H., Zhang, K., Zhu, J.K., 2019a. A model for the aberrant DNA methylomes in aging cells and cancer cells. Biochemical Society Transactions, 47(4): 997-1003.
• Zhang, Q., Zheng, S., Wang, S., Jiang, Z., Xu, S., 2019b. The effects of low selenium on DNA methylation in the tissues of chickens. Biological Trace Element Research, 191: 474-484.
• Zhao, B., Liang, R., Ge, L., Li, W., Xiao, H., Lin, H., Ruan, K., Jin, Y., 2007. Identification of drought-induced microRNAs in rice. Biochemical and Biophysical Research Communications, 354(2): 585-590.