Oxidative homeostasis of germinating wheat seeds depending on the ultrasonic effect’s duration 

Sergei S. Tarasov, Senior lecturer of the sub-department of botany, physiology and plant protection, Nizhny Novgorod State Agricultural Academy (97 Gagarina avenue, Nizhny Novgorod, Russia), E-mail: Tarasov_ss@mail.ru
Alexander P. Veselov, Doctor of biological sciences, professor, professor of the sub-department of biochemistry and biotechnology, Lobachevsky State University of Nizhny Novgorod (23 Gagarina avenue, Nizhny Novgorod, Russia), E-mail: veselov-ap@yandex.ru 

591.13:636.92+577.11 

DOI

10.21685/2307-9150-2021-3-2 

Background. Ultrasound is actively used to influence living organisms, but its physiological effect remains not fully understoodIn connection with the ability of ultrasonic waves to generate reactive oxygen species in an aqueous medium, special attention, from our point of view, should be paid to oxidative homeostasis and primary proteolysis of a reserve nutrient in germinating seeds. As the main indicators, attention should be paid to the proteins’ oxidative modification (POM), since they are the main traps of bioradicals, but their turnover in plant tissues remains unexplored. The purpose of the research is to study the effect of different times of ultrasonic exposure on the level of POM, lipid peroxidation (LPO), cysteine proteinase activity and expression of its gene (CP) in germinating wheat seeds. Materials and methods. Wheat seeds (Triticum aestivum L.), “Ekada-70” variety, collected in 2018, were used as the object of the study. The seeds were placed in an aqueous medium of an ultrasonic bath “UNITRA – UNIMA” UM – 4. The treatment was carried out for 5, 10, and 20 minutes; seeds soaked but not sonicated served as a control. At the end, the level of lipid peroxidation was determined in the seeds by the level of malonic dialdehyde (MDA) concentration, OMB registration of 2,4 – denitrophenylhydrazones (2,4 – DNPH), cysteine proteinase activity and gene expression (CP). Results. The experiments revealed the dependence of the studied parameters on the time of ultrasonic exposure. An increase in MDA content in germinating wheat seeds was shown after ultrasonic exposure. The content of 2,4 – DNPH had a wave-like dynamics, did not statistically significantly change in germinating seeds exposed to ultrasound for 5 min, increased in samples that were exposed to ultrasound for 10 min, and decreased in seeds treated with ultrasound for 20 minutes. The activity of the studied proteinase was higher in the samples after 5 minutes of ultrasonic treatment and lower than the control values in the seeds after 20 minutes of sonication. Gene expression (SR) was higher in germinating seeds subjected to 5–10 minutes ultrasonic treatment, followed by a fall below the control. Conclusions. The intensification of LPO processes, the wave-like dynamics of POM and the primary activation of proteolysis with subsequent inhibition in germinating wheat seeds after ultrasound exposure were established; protein homeostasis is more tolerant to the action of ROS compared to lipids. 

Key words

oxidative modification of proteins, lipid peroxidation, cysteine proteinases, seeds of wheat, seed germination, ultrasound 

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1. Maresca D., Lakshmanan A., Abedi M. [et al.]. Biomolecular Ultrasound and Sonogenetics. Annu Rev Chem Biomol Eng. 2018;7(9):229–252. Available at: https://doi:10.1146/annurev-chembioeng-060817-084034
2. Naeve I., Mommens M., Arukwe A., Kjørsvik E. Ultrasound as a noninvasive tool for monitoring reproductive physiology in female Atlantic salmon (Salmo salar). Physiol Rep. 2018;6(9):136–140. Available at: https://doi:10.14814/phy2.13640
3. Chen L.D., Ruan S.M., Lin Y. [et al.]. Comparison between M-score and LR-M in the reporting system of contrast-enhanced ultrasound LI-RADS. Eur Radiol. 2019;29(8): 4249–4257. Available at: https://doi:10.1007/s00330-018-5927-8
4. Methachan B., Thanapprapasr K. Polymer-Based Materials in Cancer Treatment: From Therapeutic Carrier and Ultrasound Contrast Agent to Theranostic Applications. Ultrasound Med Biol. 2017;43(1):69–82. Available at: https://doi:10.1016/j.ultrasmedbio.2016.09.009
5. Zhou L.Q., Li P., Cui X.W., Dietrich C.F. Ultrasound nanotheranostics in fighting cancer: Advances and prospects. Cancer Lett. 2020;1(470):204–219. Available at: https:// doi:10.1016/j.canlet.2019.11.034
6. Hu A., Zheng J., Qiu T. Industrial experiments for the application of ultrasound on scale control in the Chinese sugar industry. Ultrason Sonochem. 2006;13(4):329–333. Available at: https://doi:10.1016/j.ultsonch.2005.05.005
7. Alarcon-Rojo A.D., Janacua H., Rodriguez J.C. [et al.]. Power ultrasound in meat processing. Meat Sci. 2015;107:86–93. Available at: https://doi:10.1016/j.meatsci.2015. 04.015
8. Arvanitoyannis I.S., Kotsanopoulos K.V., Savva A.G. Use of ultrasounds in the food industry-Methods and effects on quality, safety, and organoleptic characteristics of foods. Crit Rev Food Sci Nutr. 2017;57(9):109–128. Available at: https://doi:10.1080/10408398.2013.860514
9. Gallo M., Ferrara L., Naviglio D. Application of Ultrasound in Food Science and Technology: A Perspective. Foods. 2018;7(10). Available at: https://doi:10.3390/foods 7100164
10. Kiss A.A., Geertman R., Wierschem M. [et al.]. Ultrasound-assisted emerging technologies for chemical processes. Chem Technol Biotechnol. 2018;93(5):1219–1227. Available at: https://doi:10.1002/jctb.5555
11. Bera S., Mondal D. A role for ultrasound in the fabrication of carbohydrate-supported nanomaterials. Ultrasound. 2019;22(2):131–156. Available at: https://doi:10.1007/ s40477-019-00363-8
12. Ribeiro F.R., Tedeschi L.O. Using real-time ultrasound and carcass measurements to estimate total internal fat in beef cattle over different breed types and managements. Anim Sci. 2012;90(9):3259–3265. Available at: https://doi:10.2527/jas.2011-4697 13. Stouffer J.R. History of ultrasound in animal science. Ultrasound Med. 2004;23(5): 577–584. Available at: https://doi:10.7863/jum.2004.23.5.577
14. Hasan M.M., Bashir T., Bae H. Use of Ultrasonication Technology for the Increased Production of Plant Secondary Metabolites. Molecules. 2017;22(7):1046. Available at: https://doi:10.3390/molecules22071046
15. Ding J., Johnson J., Chu Y.F., Feng H. Enhancement of γ-aminobutyric acid, avenanthramides, and other health-promoting metabolites in germinating oats (Avena sativa L.) treated with and without power ultrasound. Food Chemistry. 2019;283:239–247. Available at: https://doi.org/10.1016/j.foodchem.2018.12.136
16. Miano A.C., Sabadoti V.D., Augusto P.E.D. Combining Ionizing Irradiation and Ultrasound Technologies: Effect on Beans Hydration and Germination. Food Sci. 2019; 84(11):3179–3185. Available at: https://doi.org/10.1111/1750-3841.14819
17. Okada K., Kudo N., Hassan M.A. [et al.]. Threshold curves obtained under various gaseous conditions for free radical generation by burst ultrasound - Effects of dissolved gas, microbubbles and gas transport from the air. Ultrason Sonochem. 2009;16(4): 512–618. Available at: https://doi:10.1016/j.ultsonch.2008.11.010
18. Gebicka L., Gebicki J.L. The effect of ultrasound on heme enzymes in aqueous solution. Enzyme Inhib. 1997;12(2):133–141. Available at: https://doi:10.3109/1475636970 9035814
19. Ogawa R., Watanabe A., Morii A. Ultrasound up-regulates expression of heme oxygenase-1 gene in endothelial cells. Med Ultrason. 2015;42(4):467–475. Available at: https://doi:10.1007/s10396-015-0635-3
20. Jiang Z., Yao K., Yuan X. [et al.]. Effects of ultrasound treatment on physico-chemical, functional properties and antioxidant activity of whey protein isolate in the presence of calcium lactate. Sci Food Agric. 2018;98(4):1522–1529.
21. Davies M.J. Protein oxidation and peroxidation. Biochem. 2016;473(7):805–825. Available at: https://doi:10.1042/BJ20151227
22. Stal'naya I.D., Garishvili T.G. Method for determination of malonic dialdehyde. Sovremennye metody v biokhimii = Modern methods in biochemistry. Moscow: Meditsina, 1977:66–68. (In Russ.)
23. Dubinina E.E. [et al.]. Oxidative modifications of human blood serum proteins, a method for its determination. Voprosy meditsinskoy khimii = Issues of medical chemistry. 1995;41(1):24–26. (In Russ.)
24. Aleksandrova I.F., Veselov A.P., Efremenko Yu.R. Proteolytic activity of germinating wheat seeds under heat stress. Fiziologiya rasteniy = Plant physiology. 1999;46(1):223. (In Russ.)
25. Gál A.B., Carnwath J.W., Dinnyes A. [et al.]. Comparison of real-time polymerase chain reaction and end-point polymerase chain reaction for the analysis of gene expression in preimplantation embryos. Reprod Fertil Dev. 2006;18(3):365–371. doi:10.1071/rd05012
26. Kuznetsov Vl.V., Kuznetsov V.V., Romanov G.A. (eds.). Molekulyarno-geneticheskie i biokhimicheskie metody v sovremennoy biologii rasteniy = Molecular genetic and biochemical methods in modern plant biology. Moscow: BINOM. Laboratoriya znaniy, 2011:487. (In Russ.)
27. Patent CH (200410088515/8)-B 08-NOV-2004 A Triticum aestivum Cysteine Proteinase Gene and Its Utilization. Jing R., Zang Q., Guo Z., Chang X.; Chinese Academy of Agricultural Sciences; Institute of Crop Germplasm Resources.
28. Lu S. Zn2+ blocks annealing of complementary single-stranded DNA in a sequenceselective manner. Sci Rep. 2014;4:5464. Available at: https://doi:10.1038/srep05464
29. Schmittgen T.D., Zakrajsek B.A., Mills A.G. [et al.]. Quantitative reverse transcriptionpolymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal Biochem. 2000;285(2):194–204. doi:10.1006/abio.2000.4753
30. Glants S. Mediko-biologicheskaya statistika = Biomedical statistics. Moscow: Praktika, 1999:459. (In Russ.)
31. Dubinina E.E. Produkty metabolizma kisloroda v funktsional'noy aktivnosti kletok = Oxygen metabolism products in the functional activity of cells. Saint-Petersburg, 2006: 396. (In Russ.)
32. Jung T., Höhn A., Grune T. The proteasome and the degradation of oxidized proteins: Part II - protein oxidation and proteasomal degradation. Redox Biol. 2014;2:99–104. Available at: https://doi:10.1016/j.redox.2013.12.008
33. Raynes R., Pomatto L.C., Davies K.J. Degradation of oxidized proteins by the proteasome: Distinguishing between the 20S, 26S, and immunoproteasome proteolytic pathways. Mol Aspects Med. 2016;50:41–55. Available at: https://doi:10.1016/j.mam. 2016.05.001
34. He L.L., Wang X., Wu X.X. [et al.]. Protein damage and reactive oxygen species generation induced by the synergistic effects of ultrasound and methylene blue. Spectrochim Acta A Mol Biomol Spectrosc. 2015;134:361–366. Available at: https://doi:10.1016/ j.saa.2014.06.121
35. Duco W., Grosso V., Zaccari D., Soltermann A.T. Generation of ROS mediated by mechanical waves (ultrasound) and its possible applications. Methods. 2016;109:141–148. Available at: https://doi:10.1016/j.ymeth.2016.07.015
36. Jia C., Xu L., Han T. [et al.]. Generation of Reactive Oxygen Species in Heterogeneously Sonoporated Cells by Microbubbles with Single-Pulse Ultrasound. Ultrasound Med Biol. 2018;44(5):1074–1085. Available at: https://doi:10.1016/j.ultrasmedbio.2018. 01.006
37. Escoffre J.M., Campomanes P., Tarek M., Bouakaz A. New insights on the role of ROS in the mechanisms of sonoporation-mediated gene delivery. Ultrason Sonochem. 2020; 64:1049–1098. Available at: https://doi:10.1016/j.ultsonch.2020.104998
38. Giuntini F., Foglietta F., Marucco A.M. [et al.]. Insight into ultrasound-mediated reactive oxygen species generation by various metal-porphyrin complexes. Free Radic Biol Med. 2018;121:190–201. Available at: https://doi:10.1016/j.freeradbiomed.2018.05.002
39. Wang P., Wang X., Zhang K. [et al.]. The spectroscopy analyses of PpIX by ultrasound irradiation and its sonotoxicity in vitro. Ultrasonics. 2013;53(5):935–942. Available at: https://doi:10.1016/j.ultras.2012.10.019
40. Zhang K., Xu H., Jia X. [et al.]. Ultrasound-Triggered Nitric Oxide Release Platform Based on Energy Transformation for Targeted Inhibition of Pancreatic Tumor. ACS Nano. 2016;10(12):10 816–10 828. Available at: https://doi:10.1021/acsnano.6b04921
41. Lane B.G. Cellular desiccation and hydration: developmentally regulated proteins, and the maturation and germination of seed embryos. FASEB. 1991;5(14):2893–2901. Available at: https://doi:10.1096/fasebj.5.14.175235
42. Liu Y., Han C., Deng X. [et al.]. Integrated physiology and proteome analysis of embryo and endosperm highlights complex metabolic networks involved in seed germination in wheat (Triticum aestivum L.). Plant Physiol. 2018;229:63–76. Available at: https://doi:10.1016/j.jplph.2018.06.011
43. Yadav S.P., Ahuja V.P., Das H.K. Changes in amino acid composition of proteins in developing wheat embryo during seed germination. Indian J. Biochem Biophys. 1972; 9(4):350–351.
44. Lowe L.B., Ries S.K. Endosperm protein of wheat seed as a determinant of seedling growth. Plant Physiol. 1973;51(1):57–60. Available at:https://doi:10.1104/pp.51.1.57