Hydrogen peroxide promotes metabolic changes and alleviates effects of static magnetic field on tobacco cells

Document Type : Original Article

Authors

1 Department of Plant Biology, Faculty of Biological Science, Tarbiat Modares University (TMU), POB 14115-154, Tehran, Iran

2 Department of Physics, Faculty of Basic Science, Shahed University, Tehran, Iran

3 Department of Biological Science, Farhangian University, Tehran, Iran

10.22034/ijpp.2021.1935207.1342

Abstract

Plant cells metabolism is known to undergo considerable reprogramming in response to static magnetic field (SMF). In the present research changes of metabolism induced by SMF and underlying mechanism(s) was investigated in suspension-cultured tobacco (Nicotiana tabacum cv. Barley 21) cells. Sugars and amino acids were monitored by HPLC, components of redox system were measured by spectrophotometer and expression of genes was evaluated by RT-PCR. Exposure to SMF decreased the adenosine triphosphate, glucose, fructose, and sucrose contents but increased hydrogen peroxide, nitric oxide, hydroxyl radical, proline, and reduced glutathione (GSH). Treatment with SMF also increased the gene expression and activity of catalase, compared to the control group. Exposure to SMF also increased the contents of phenylalanine and tyrosine, elevated the gene expression and activity of phenylalanine ammonia-lyase, and subsequently increased soluble phenolic compounds. Pretreatment of the cells with 40 µM sodium ascorbate reduced all above mentioned parameters except for nitric oxide and hydroxyl radical contents. The rate of membrane lipid peroxidation was also increased in ascorbate-pretreated cells. The results suggest a crucial role for H2O2 in triggering changes in primary and secondary metabolic pathways which result in alleviation of stress of SMF in tobacco cells.

Keywords


Abdollahi, F., H. Amiri, V. Niknam, F. Ghanati,  and K. Mahdigholi. 2019. Effects of Static Magnetic Fields on the Antioxidant System of Almond Seeds. Russian Journal of Plant Physiology, 66: 299-307.
Akkol, EK., F. Goger, M. Koşar and KHC. Başer. 2008. Phenolic composition and biological activities of Salvia halophila and Salvia virgata from Turkey. Food Chemistry, 108: 942-949.
Bates, LS., R. P. Waldren, and ID Teare. 1973. Rapid determination of free proline for water-stress studies. Plant Soil, 39: 205-207.
Akram, NA., F. Shafiq, and M. Ashraf. 2017. Ascorbic acid-a potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Frontiers in Plant Science, 613(8):1-17.
Bradford, MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248-254.
Calabro, E.,S. Condello, M. Curro, N. Ferlazzo, D. Caccamo, S. Magazu, and R. Ientile. 2013. Effects of low intensity static magnetic field on FTIR spectra and ROS production in SH‐SY5Y neuronal‐like cells. Bioelectromagnetics, 34: 618-629.
Davey, MW., MV. Managu, I. Dirk, S. Maite, K. Angelos, N. Smirnoff, IJJ Binenzir, JJ. Strain, D. Favell, and J. Fletcher.2000. Plant Ascorbic acid: chemistry, function, metabolism, bioavailability, and effects of processing. Journal of the Science of Food and Agriculture, 80: 825–860.
De Gara, L., MC. de Pinto, and O. Arrigoni.1997. Asc.orbate synthesis and Ascorbate peroxidase activity during the early stage of wheat germination. Physiologia Plantarum, 100: 894–90.
De Vos, CHR., H.  Scha,t, MAM. De Waal, R. Vooijs, and WHO. Ernst. 1991. Increased resistance to copper‐induced damage of the root cell plasmalemma in copper tolerant Silene cucubalus. Physiologia Plantarum, 82: 523-528.
Farnese, FS., PE. Menezes-Silva, GS. Gusman, and JA. Oliveira. 2016. When bad guys become good ones: the key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress. Frontiers in Plant Science, 7: 471.
Foyer, CH. And G. Noctor. 2005. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell, 17:1866–1875.
Garg, N. and H. Kaur. 2012. Influence of zinc on cadmium-induced toxicity in nodules of pigeon pea (CajanuscajanL. Millsp.) inoculated with arbuscular mycorrhizal (AM) fungi. Acta Physiologiae Plantarum, 34: 1363-1380.
Ghanati, F., P. Abdolmaleki, M. Vaezzadeh, E. Rajabbeigi, and M. Yazdani. 2007. Application of magnetic field and iron to change medicinal products of Ocimum basilicum. Environmentalist, 27: 429-434.
Gill, SS. and N. Tuteja. 2010.Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48: 909–930.
Haghighat, N.,P. Abdolmaleki, F. Ghanati, M. Behmanesh, and A. Payez, A. 2014. Modification of catalase and MAPK in Vicia faba cultivated in soil with high natural radioactivity and treated with a static magnetic field. Journal of Plant Physiology, 171: 99-103.
Green, LC., DA. Wagner, J. Glogowski, PL. Skipper, JS. Wishnok, and SR. Tannenbaum. 1982.Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Analytical Biochemistry, 126: 131-138.
Hildebrandt, TM., AN. Nesi, WL. Araujo, and HP. Braun. 2015. Amino acid catabolism in plants. Molecular plant, 8: 1563-1579.
Jouni, FJ., P. Abdolmaleki, and F. Ghanati. 2012.Oxidative stress in broad bean (Vicia faba L.) induced by static magnetic field under natural radioactivity. Mutation Research/ Genetic Toxicology and Environmental Mutagenesis, 741: 116–121.
Leon, J., A. Costa, and MC. Castillo. 2016.Nitric oxide triggers a transient metabolic reprogramming in Arabidopsis. Scientific Reports, 6: 37945.
Maffei, ME. 2014. Magnetic field effects on plant growth, development, and evolution. Frontiers in Plant Science, 5: 445.
Mohammadi, F., F. Ghanati, M. Sharifi, and N. Ahmadian Chashmi. 2018. On the mechanism of the cell cycle control of suspension-cultured tobacco cells after exposure to the static magnetic field. Plant Science, 277: 139-144.
Nahidian, B., F. Ghanati, M. Shahbazi, and N. Soltani. 2018. Effect of nutrients on the growth and physiological features of newly isolated Haematococcus Pluvialis TMU1. Bioresource Technology, 255: 229-237.
Nemati, F., F.  Ghanati, H. Ahmadi Gavlighi, and M. Sharifi. 2018. Fructan dynamics and antioxidant capacity of 4-day-old seedlings of wheat (Triticum aestivum) cultivars during drought stress and recovery. Functional Plant Biology, 45: 1000-1008.
Okano, H., H. Masuda, and C. Ohkubo. 2005. Decreased plasma levels of nitric oxide metabolites, angiotensin II, and aldosterone in spontaneously hypertensive rats exposed to 5 mT static magnetic field. Bioelectromagnetics, 26: 161-172.
Pormehr, M., F. Ghanati, M. Sharifi, PF. McCabe, S. Hosseinkhani, and H. Zare-Maivan. 2019. The role of SIPK signaling pathway in antioxidant activity and programmed cell death of tobacco cells after exposure to cadmium. Plant Science, 280: 416-423.
Sahebjamei, H.,P. Abdolmaleki, and F. Ghanati. 2007. Effects of magnetic field on the antioxidant enzyme activities of suspension‐cultured tobacco cells. Bioelectromagnetics, 28: 42-47.
Santos, LO., RM. Alegre, C. Garcia-Diego, and J. Cuellar. 2010.Effects of magnetic fields on biomass and glutathione production by the yeast Saccharomyces cerevisiae. Process Biochemistry, 45: 1362-1367.
Shang, GM., JC. Wu, and YJ. Yuan. 2004. Improved cell growth and Taxol production of suspension-cultured Taxus chinensis var. mairei in alternating and direct current magnetic fields. Biotechnology Letters, 26: 875-878.
Shokrollahi, S., F. Ghanati, RH. Sajedi, and M. Sharifi. 2018. Possible role of iron-containing proteins in physiological responses of soybean to the static magnetic field. Journal of Plant Physiology, 226: 163-171.
Smal,l DP., NP. Hüner, and W. Wan. 2012. Effect of static magnetic fields on the growth, photosynthesis, and ultrastructure of Chlorella kessleri microalgae. Bioelectromagnetics, 33: 298-308.
Taghizadeh, M., F. Nasibi, K.M. Kalantari, and F. Ghanati. 2019.Evaluation of secondary metabolites and antioxidant activity in Dracocephalum polychaetum Bornm. cell suspension culture under magnetite nanoparticles and static magnetic field elicitation. Plant Cell, Tissue and Organ Culture, 1-10.
Tzin, V. and G. Galili. 2010. The biosynthetic pathways for shikimate and aromatic amino acids in Arabidopsis thalianaThe Arabidopsis Book, 8: e0132.
Velikova, V., I. Yordanov, and A. Edreva. 2000. Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Science, 15159: e66.
Vergallo, C., M. Ahmadi, H. Mobasheri, and L. Dini. 2014. Impact of inhomogeneous static magnetic field (31.7–232.0 mT) exposure on human neuroblastoma SH-SY5Y cells during cisplatin administration. PloS One, 9: e113530.
Wang, H. and X. Zhang. 2017. Magnetic fields and reactive oxygen species. International Journal of Molecular Science, 18: 2175.
Wang, JW., LP. Zheng, JY. Wu. and RX. Tan. 2006. Involvement of nitric oxide in the oxidative burst, phenylalanine ammonia-lyase activation, and Taxol production induced by low-energy ultrasound in Taxus yunnanensis cell suspension cultures. Nitric Oxide 15: 351-358.
Zafari, S., M. Sharifi, N. Ahmadian Chashmi, and LA. Mur. 2016. Modulation of Pb-induced stress in Prosopis shoots through an interconnected network of signaling molecules, phenolic compounds, and amino acids. Plant Physiology and Biochemistry, 99: 11-20.
Zafari, S., M. Sharifi, and LA. Mur. and NA. Chashmi. 2017. Favoring NO over H2O2 production will increase Pb tolerance in Prosopis farcta via altered primary metabolism. Ecotoxicology and Environmental safety, 142: 293-302.
Zhang, X., H. Ma, H. Qi, and J. Zhao. 2014. Roles of hydroxyproline-rich glycoproteins in the pollen tube and style cell growth of tobacco (Nicotiana tabacum L.). Journal of Plant Physiology, 171: 1036–1045.