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Hormetic Effects of Low Dose Gamma Irradiation on Antioxidant Defense System and Thymol Biosynthesis in Thyme Plants

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Abstract

This study investigated the impact of different doses (0, 1, 3, and 5 Gy) of gamma radiation on antioxidant mechanisms and thymol biosynthesis in Thymus vulgaris. Concentration of hydrogen peroxide (H2O2) and malondialdehyde (MDA) exhibited dose-dependent increases, indicating oxidative damage and a time-dependent progression of stress. Superoxide dismutase (SOD) activities were triggered in response, accompanied by time-dependent variations in peroxidase (POD) and polyphenol oxidase (PPO) activities. Biochemical analyses revealed enhanced total phenolic content (TPC), total flavonoid content (TFC) and anthocyanin levels at 1 Gy. Additionally, the effect of radiation on the expression of pivotal genes in the biosynthesis pathway of thymol, such as DXR, TvTPS, and CYP71D178, was investigated. Gamma irradiation significantly up-regulated DXR transcription at higher doses, while TvTPS and CYP71D178 transcription peaked at 1 Gy. Thymol emerged as the predominant compound in the essential oil composition, experiencing a significant increase at 1 Gy, thus illustrating a hormetic response. This study provides scientific insights into the hormesis effects of gamma irradiation on antioxidant responses and thymol biosynthesis in Thymus vulgaris, contributing to a better understanding of the complicated biochemical processes involved in plant adaptation to radiation stress.

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REFERENCES

  1. Villegas, D., Sepúlveda, C., and Ly, D., Use of low-dose gamma radiation to promote the germination and early development in seeds, Seed Biology – New Advances, IntechOpen, 2023, https://doi.org/10.5772/intechopen.1003137

    Book  Google Scholar 

  2. Kitara, P., Pandey, N., and Keshavkant, S., Gamma radiation: A potential tool for abiotic stress mitigation and management of agroecosystem, Plant Stress, 2022, vol. 5, p. 100089. https://doi.org/10.1016/j.stress.2022.100089

    Article  CAS  Google Scholar 

  3. Tan, Y., Duan, Y., Chi, Q., Wang, R., Yin, Y., Cui, D., Li, S., Wang, A., Ma, R., Li, B., Jiao, Z., and Sun, H., The role of reactive oxygen species in plant response to radiation, Int. J. Mol. Sci., 2023, vol. 24, p. 3346. https://doi.org/10.3390/ijms24043346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Choi, H.I., Han, S.M., Jo, Y.D., Hong, M.J., Kim, S.H., and Kim, J.B., Effects of acute and chronic gamma irradiation on the cell biology and physiology of rice plants, Plants, 2021, vol. 10, p. 439. https://doi.org/10.3390/plants10030439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Volkova, P.Y., Bondarenko, E.V., and Kazakova, E.A., Radiation hormesis in plants, Curr. Opin. Toxicol., 2022, vol. 30, p. 100334. https://doi.org/10.1016/j.cotox.2022.02.007

    Article  CAS  Google Scholar 

  6. Al-Khayri, J.M., Rashmi, R., Toppo, V., Chole, P.B., Banadka, A., Sudheer, W.N., Nagella, P., Shehata, W.F., Al-Mssallem, M.Q., Alessa, F.M., and Almaghasla, M.I., Plant secondary metabolites: The Weapons for biotic stress management, Metabolites, 2023, vol. 13, p. 716.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Elshafie, H.S., Camele, I., and Mohamed, A.A., A comprehensive review on the biological, agricultural and pharmaceutical properties of secondary metabolites based-plant origin, Int. J. Mol. Sci., 2023, vol. 24, p. 3266. https://doi.org/10.3390/ijms24043266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kumar, S., Saini, R., Suthar, P., Kumar, V., and Sharma, R., Plant secondary metabolites: Their food and therapeutic importance, in Plant Secondary Metabolites: Physico-chemical Properties and Therapeutic Applications, Sharama, A.K. and Sharma A., Eds., Singapore: Springer Nature Singapore, 2022, p. 371. https://doi.org/10.1007/978-981-16-4779-6_12

    Book  Google Scholar 

  9. Posgay, M., Greff, B., Kapcsándi, V., and Lakatos, E., Effect of Thymus vulgaris L. essential oil and thymol on the microbiological properties of meat and meat products: A review, Heliyon, 2022, vol. 8, p. 10812. https://doi.org/10.1016/j.heliyon.2022.e10812

    Article  CAS  Google Scholar 

  10. Biswal, R.A. and Pazhamalai, V., A Centum of Valuable Plant Bioactives, Mushtaq, M. and Anwar, F., Eds., Academic Press, 2021, p. 275. https://doi.org/10.1016/B978-0-12-822923-1.00015-7

    Book  Google Scholar 

  11. Masocatto, D.C., Matsumoto, M.A., Coelho, T.M.K., Jardim, E.C.G., de Mendonça, J.C.G., da Silva, J.C.L., Carollo, C.A., Carollo, A.R., Marques, M.C.S., Fernandes, S.M., and Hassumi, J.S., Comparison of antimicrobial activity of thymol and carvacrol to chlorhexidine in surgery, Res. Soc. Dev., 2021, vol. 10, p. 4310716310. https://doi.org/10.33448/rsd-v10i7.16310

    Article  Google Scholar 

  12. Dobler, D., Runkel, F., and Schmidts, T., Effect of essential oils on oral halitosis treatment: A review, Eur. J. Oral. Sci., 2020, vol. 128, p. 476. https://doi.org/10.1111/eos.12745

    Article  CAS  PubMed  Google Scholar 

  13. Kowalczyk, A., Przychodna, M., Sopata, S., Bodalska, A., and Fecka, I., Thymol and thyme essential oil—new insights into selected therapeutic applications, Molecules, 2020, vol. 25, p. 4125. https://doi.org/10.3390/molecules25184125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Krause, S.T., Liao, P., Crocoll, C., Boachon, B., Förster, C., Leidecker, F., Wiese, N., Zhao, D., Wood, J.C., Buell, C.R., and Gershenzon, J., The biosynthesis of thymol, carvacrol, and thymohydroquinone in Lamiaceae proceeds via cytochrome P450s and a short-chain dehydrogenase, PNAS, 2021, vol. 118, p. 2110092118. https://doi.org/10.1073/pnas.2110092118

    Article  CAS  Google Scholar 

  15. Mohammadi, V., Talebi, S., Ahmadnasab, M., and Mollahassanzadeh, H., The effect of induced polyploidy on phytochemistry, cellular organelles and the expression of genes involved in thymol and carvacrol biosynthetic pathway in thyme (Thymus vulgaris), Front. Plant Sci., 2023, vol. 14, p. 1228844. https://doi.org/10.3389/fpls.2023.1228844

    Article  PubMed  PubMed Central  Google Scholar 

  16. Bradford, M. M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, vol. 72, p. 248. https://doi.org/10.1016/0003-2697(76)90527-3

    Article  CAS  PubMed  Google Scholar 

  17. Giannopolitis, C.N. and Ries, S.K., Superoxide dismutases: II. Purification and quantitative relationship with water-soluble protein in seedlings, Plant Physiol., 1977, vol. 59, p. 315. https://doi.org/10.1104/pp.59.2.309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Cheng, G.W. and Breen, P.J., Activity of phenylalanine ammonia-lyase (PAL) and concentrations of anthocyanins and phenolics in develo** strawberry fruit, J. Am. Soc. Hortic. Sci., 1991, vol. 116, p. 865. https://doi.org/10.21273/JASHS.116.5.865

    Article  CAS  Google Scholar 

  19. Zhou, B., Wang, J., Guo, Z., Tan, H., and Zhu, X., A simple colorimetric method for determination of hydrogen peroxide in plant tissues, Plant Growth Regul., 2006, vol. 49, p. 113. https://doi.org/10.1007/s10725-006-9000-2

    Article  CAS  Google Scholar 

  20. Blainski, A., Lopes, G.C., and De Mello, J.C.P., Application and analysis of the folin ciocalteu method for the determination of the total phenolic content from Limonium brasiliense L. Molecules, 2013, vol. 18, p. 6852. https://doi.org/10.3390/molecules18066852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Chang, C.-C., Yang, M.-H., Wen, H.-M., and Chern, J.-C., Estimation of total flavonoid content in propolis by two complementary colorimetric methods, J. Food Drug Anal., 2002, vol. 10, p. 3. https://doi.org/10.38212/2224-6614.2748

    Article  Google Scholar 

  22. Ni, J., Zhao, Y., Tao, R., Yin, L., Gao, L., Strid, A., Qian, M., Li, J., Li, Y., Shen, J., Teng, Y., and Bai, S., Ethylene mediates the branching of the jasmonate-induced flavonoid biosynthesis pathway by suppressing anthocyanin biosynthesis in red Chinese pear fruits, Plant Biotechnol. J., 2020, vol. 18, p. 1223. https://doi.org/10.1111/pbi.13287

    Article  CAS  PubMed  Google Scholar 

  23. Sachdev, S., Ansari, S.A., Ansari, M.I., Fujita, M., and Hasanuzzaman, M., Abiotic stress and reactive oxygen species: Generation, signaling, and defense mechanisms, Antioxidants, 2021, vol. 10, p. 277. https://doi.org/10.3390/antiox10020277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Dvořák, P., Krasylenko, Y., Zeiner, A., Šamaj, J., and Takáč, T., Signaling toward reactive oxygen species-scavenging enzymes in plants, Front. Plant Sci., 2021, vol. 11, p. 618835. https://doi.org/10.3389/fpls.2020.618835

    Article  PubMed  PubMed Central  Google Scholar 

  25. Zhang, S., Recent advances of polyphenol oxidases in plants, Molecules, 2023, vol. 28, p. 2158. https://doi.org/10.3390/molecules28052158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Rajput, V.D., Harish, Singh, R.K., Verma, K.K., Sharma, L., Quiroz-Figueroa, F.R., Meena, M., Gour, V.S., Minkina, T., Sushkova, S., and Mandzhieva, S., Recent developments in enzymatic antioxidant defence mechanism in plants with special reference to abiotic stress, Biology, 2021, vol. 10, p. 267. https://doi.org/10.3390/biology10040267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Yasmin, K., Arulbalachandran, D., Soundarya, V., and Vanmathi, S., Effects of gamma radiation (γ) on biochemical and antioxidant properties in black gram (Vigna mungo L. Hepper), Int. J. Radiat. Biol., 2019, vol. 95, p. 1135. https://doi.org/10.1080/09553002.2019.1589022

    Article  CAS  PubMed  Google Scholar 

  28. Hussein, H.A.A., Influence of radio-grain priming on growth, antioxidant capacity, and yield of barley plants, Biotechnol. Rep., 2022, vol. 34, p. e00724. https://doi.org/10.1016/j.btre.2022.e00724

    Article  CAS  Google Scholar 

  29. Huang, H., Ullah, F., Zhou, D.X., Yi, M., and Zhao, Y., Mechanisms of ROS regulation of plant development and stress responses, Front. Plant Sci., 2019, vol. 10, p. 800. https://doi.org/10.3389/fpls.2019.00800

    Article  PubMed  PubMed Central  Google Scholar 

  30. Ashraf, M.A., Riaz, M., Arif, M.S., Rasheed, R., Iqbal, M., Hussain, I., and Mubarik, M.S., The role of non-enzymatic antioxidants in improving abiotic stress tolerance in plants, in Plant Tolerance to Environmental Stress, CRC Press, 2019, p. 129.

    Google Scholar 

  31. Sharma, A., Shahzad, B., Rehman, A., Bhardwaj, R., Landi, M., and Zheng, B., Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress, Molecules, 2019, vol. 24, p. 2452. https://doi.org/10.3390/molecules24132452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Harrison, K. and Were, L.M., Effect of gamma irradiation on total phenolic content yield and antioxidant capacity of almond skin extracts, Food Chem., 2007, vol. 102, p. 932. https://doi.org/10.1016/j.foodchem.2006.06.034

    Article  CAS  Google Scholar 

  33. Lee, S.C., Jeong, S.M., Kim, S.Y., Park, H.R., Nam, K.C., and Ahn, D.U., Effect of far-infrared radiation and heat treatment on the antioxidant activity of water extracts from peanut hulls, Food Chem., 2006, vol. 94, p. 489. https://doi.org/10.1016/j.foodchem.2004.12.001

    Article  CAS  Google Scholar 

  34. Jamshidi, M., Barzegar, M., and Sahari, M.A., Effect of gamma and microwave irradiation on antioxidant and antimicrobial activities of Cinnamomum zeylanicum and Echinacea purpurea, Int. Food Res. J., 2014, vol. 21, p. 1289.

    Google Scholar 

  35. Kaur, S., Tiwari, V., Kumari, A., Chaudhary, E., Sharma, A., Ali, U., and Garg, M., Protective and defensive role of anthocyanins under plant abiotic and biotic stresses: An emerging application in sustainable agriculture, J. Biotech., 2023, vol. 361, p. 12. https://doi.org/10.1016/j.jbiotec.2022.11.009

    Article  CAS  Google Scholar 

  36. Aly, A., Eliwa, N., Taha, A., and Borik, Z., Physiological and biochemical markers of gamma irradiated white radish (Raphanus sativus), Int. J. Radiat. Biol., 2023, vol. 99, p. 1413. https://doi.org/10.1080/09553002.2023.2176561

    Article  CAS  PubMed  Google Scholar 

  37. Hanafy, R.S. and Akladious, S.A., Physiological and molecular studies on the effect of gamma radiation in fenugreek (Trigonella foenum-graecum L.) plants, J. Genet. Eng. Biotechnol., 2018, vol. 16, p. 683. https://doi.org/10.1016/j.jgeb.2018.02.012

    Article  PubMed  PubMed Central  Google Scholar 

  38. Stahl-Biskup, E. and Sáez, F., Thyme: the Genus Thymus, CRC Press, 2002. https://doi.org/10.4324/9780203216859

    Book  Google Scholar 

  39. Majdi, M., Malekzadeh-Mashhady, A., Maroufi, A., and Crocoll, C., Tissue-specific gene-expression patterns of genes associated with thymol/carvacrol biosynthesis in thyme (Thymus vulgaris L.) and their differential changes upon treatment with abiotic elicitors, Plant Physiol. Biochem., 2017, vol. 115, p. 152. https://doi.org/10.1016/j.plaphy.2017.03.016

    Article  CAS  PubMed  Google Scholar 

  40. Kianersi, F., Pour-Aboughadareh, A., Majdi, M., and Poczai, P., Effect of methyl jasmonate on thymol, carvacrol, phytochemical accumulation, and expression of key genes involved in thymol/carvacrol biosynthetic pathway in some iranian thyme species, Int. J. Mol. Sci., 2021, vol. 22, p. 11124. https://doi.org/10.3390/ijms222011124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

Authors would like to thank Hamed Askari and Dr. Nahid Hajiloo for assistance in conducting work.

Funding

This work was supported by the National Institute of Genetic Engineering and Biotechnology (NIGEB) and Nuclear Science and Technology Research Institute (project no. 804).

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Authors and Affiliations

  1. Department of Plant Bioproducts, Agricultural Biotechnology Research Institute, National Institute of Genetic Engineering and Biotechnology, Tehran, Iran

    M. Norouzi & F. Sanjarian

  2. Nuclear Agriculture Research School, Nuclear Science and Technology Research Institute (NSTRI), Atomic Energy Organization of Iran (AEOI), Karaj, Iran

    S. Shahbazi

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FS and SS designed the experiments. MN collected samples and performed the experiments. FS and MN drafted the manuscript and all authors revised it.

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Correspondence to F. Sanjarian.

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Norouzi, M., Sanjarian, F. & Shahbazi, S. Hormetic Effects of Low Dose Gamma Irradiation on Antioxidant Defense System and Thymol Biosynthesis in Thyme Plants. Russ J Plant Physiol 71, 44 (2024). https://doi.org/10.1134/S1021443724603914

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