Effects of silicon on glycine-betaine, phytochelatin, and antioxidant enzymes in licorice (Glycyrrhiza glabra L.) under aluminum stress

Subject Areas : Plant Physiology

Mojtaba  Yazdani ¹ (Department of Biology, Islamic Azad University, Ashtian Branch, Ashtian, Iran)
Shekoofeh  Enteshari ² (Department of Biology, Payame Noor University, Iran)
Sara  Saadatmand ³ (Department of Biology, Science and Research Branch, Islamic Azad University, Tehran, Iran)
Saeid  Habibollahi ⁴ (Department of Chemistry, Payame Noor University, Tehran, Iran)

Received: 2021-05-04 Accepted : 2021-05-09 Published : 2021-01-01

Keywords: antioxidant enzyme, licorice, aluminum stress, phytochelatin, glycine-betaine,

Abstract :

Licorice (Glycyrrhiza glabra L.) is a valuable plant for the treatment of several diseases. Negative effects of aluminum stress on plants have been reported and silicon may alleviate these negative effects through promoting antioxidant system. This study was conducted to investigate the effects of silicon on glycine-betaine, phytochelatin, and antioxidant parameters in licorice plant under aluminum stress. The plants were treated with silicon (0, 0.5, and 1.50 mM) and submitted to aluminum stress (100, 250, and 400 µM). Glycine-betaine contents of roots and shoots were investigated. Also, guaiacol peroxidase (GPx), peroxidase (POX), superoxide dismutase (SOD), phenylalanine ammonia lyase (PAL), 2,2-Diphenyl-1-picrylhydrazyl (DPPH) radical scavenging activities, and hydrogen peroxide (H2O2) and root phytochelatin were assessed after treatment with aluminum. Results showed that aluminum stress increased the contents of glycine-betaine and root phytochelatin, activities of GPx, POX, SOD, PAL, DPPH radical scavenging, and H2O2 content (p <0.05). Application of silicon application also increased the contents of glycine-betaine, activities of GPx, POX, PAL, DPPH radical scavenging, and root phytochelatin (p <0.05) while it decreased H2O2 and SOD contents (p <0.05). Based on the findings, application of silicon is recommended for protection of licorice under aluminum stress.

References:

 

Abe, N., T. Murata and A. Hirota, 1998. 'Novel 1,1-diphenyl-2-picryhy- drazylradical scavengers, bisorbicillin and demethyltrichodimerol, from a fungus'. Bioscience, Biotechnology and Biochemistry. 62: 61-662.

Ahanger, M.A., N.A. Akram, M. Ashraf, M.N. Alyemeni, L. Wijaya and P. Ahmad, 2017. 'Plant responses to environmental stresses, from gene to biotechnology'. AoB PLANTS.   9(4), plx025, https://doi.org/10.1093/aobpla

Ahmadi, N., H. Hassanpour, M. Hekmati, and M. Ghanbarzadeh, 2020. 'Effect of SiO₂ nanoparticles on phytochemical and anatomical alterations in Anthemis gilanica'. Iranian Journal of Plant Physiology 10 (3): 3223-3231.

Ali S., Z. Abbas, M.F. Seleiman, M. Rizwan, B. Ahmed Alhammad, A. Shami, M. Hasanuzzaman and D. Kalderis, 2020. 'Glycine betaine accumulation, significance and interests for heavy metal tolerance in plants'. Plants, 9 (7): 896. doi: 10.3390/plants9070896.

Amara H., M. Lelu-Walter, V. Gloaguen and C. Faugeron-Girard, 2020. 'Tolerance of douglas fir somatic plantlets to aluminum stress: biological, cytological, and mineral studies'. Plants, 9 9(4): 536.  https://dx.doi.org/10.3390/plants9040536.

Bari M.A., S.A. Prity, U. Das, M.S. Akther, S.A. Sajib, M.A. Reza and A.H. Kabir, 2020. 'Silicon induces phytochelatin and ROS scavengers facilitating cadmium detoxification in rice'. Plant Biology. 22: 472–479.

Behdad A., S. Mohsenzadeh, M. Azizi and N. Moshtaghi, 2020. 'Salinity effects on physiological and phytochemical characteristics and gene expression of two Glycyrrhiza glabra L. populations'. Phytochemistry. 171:112236 https://doi.org/10.1016/j.phytochem.2019.112236

Bhat, J.A., S.M. Shivaraj, P. Singh, D.B. Navadagi, D.K. Tripathi, P.K. Dash, A.U. Solanke, H. Sonah and R. Deshmukh, 2019. 'Role of Silicon in Mitigation of Heavy Metal Stresses in Crop Plants'. Plants (Basel). 8(3): 71. https://dx.doi.org/10.3390/plants8030071.

Bojórquez-Quintal, E., C. Escalante-Magaña, I. Echevarría-Machado and M. Martínez-Estévez, 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.

Caretto S., V. Linsalata, G. Colella, G. Mita and V. Lattanzio, 2015. 'Carbon fluxes between primary metabolism and phenolic pathway in plant tissues under stress'. Int. J. Mol. Sci.16: 26378–26394.

Chalmardi, Z.K., A. Abdolzadeh and H.R. Sadeghipour, 2013. 'Silicon nutrition potentiates the antioxidant metabolism of rice plants under iron toxicityl. Acta Physiol. Plant. 36: 493–502.

Chance, B. and A.C. Maehly, 1995. 'An assay of catalase and peroxidase'. In: Method in Enzymology, Colowick, S. P., N.D. Kapland, (eds), Academic Press, New York, pp. 764–791.

De Vos C.H., M.J. Vonk, R. Vooijs and H. Schat, 1992. 'Glutathione deplation due to copper inducedphytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol. 98: 853-858.

Delavar,K., F. Ghanati, H. Zare-Maivan and M. Behmanesh, 2016. 'The effect of the silicon and aluminum interaction on the physiological parameters of maize'. Iranian Journal of Plant Physiology. 6(4):1785-1794.

Delhaize, E., J.F. Ma and P.R. Ryan, 2012. 'Transcriptional regulation of aluminum tolerance genes'. Trend Plant Sci. 17: 341–348.

Dubey, A.K., 2014. 'The role of silicon in suppressing paddy diseases'. Asian journal of
multidiplinary studies. 2(10):172-176.

Elisa, A.A., S. Ninomiya, J. Shamshuddin and I. Roslan, 2016. 'Alleviating aluminum toxicityin an acid sulfate soil from Peninsular Malaysia by calcium silicate application. Solid Earth. 7: 367–374.

Emamverdian A, Y. Ding, Y. Xie and S. Sangari, 2018. 'Silicon mechanisms to ameliorate heavy metal stress in plants'. BioMed Research International. Article ID 8492898, https://doi.org/10.1155/2018/8492898.

Enteshari, S. ,R. Alishavandi and K. Delavar. 2011. 'Interactive effects of silicon and NaCl on the some physiologicaland biochemical parameters in Borago officinalis L'. Iranian Journal of Plant Physiology,2(1): 315‐320.

Esmaeili H., A. Karami, J. Hadian, M.J. Saharkhiz and S.N. Ebrahimi, 2019. 'Variation in the phytochemical contents and antioxidant activity of Glycyrrhiza glabra populations collected in Iran'. Ind. Crop Prod. 137: 248–259.

Farag M.A., A. Porzel and L.A. Wessjohann, 2012. 'Comparative metabolite profiling and fingerprinting of medicinal licorice roots using a multiplex approach of GC–MS, LC–MS and 1D NMR techniques'. Phytochemistry. 76:60–72.

Fryzova, R., M. Pohanka, P. Martinkova, H. Cihlarova, M. Brtnicky and J. Hladky, 2017. 'Oxidative Stress and Heavy Metals in Plants' in: Reviews of Environmental Contamination and Toxicology, Vol. 2454, G. W. Ware (ed). (New York: Springer International Publishing), 129- 156. https://doi. org/10.1007/ 398_2017_ 7.

Gagoonani, S., S. Enteshari, K. Delavar and M. Behyar. 2011. 'Interactive effects of silicon and aluminum on the malondialdehyde (MDA), proline, protein and phenolic compounds in Borago officinalis L'. J. Med. Plants Res.,5: 5818–5827.

Gallo-Franco J.J., C.C. Sosa, T. Ghneim-Herrera and M. Quimbaya, 2020. 'Epigenetic control of plant response to heavy metal stress: A new view on aluminum tolerance'. Front. Plant Sci. 11: 602-625 . 

Ghori N.H., T. Ghori, M.Q. Hayat, S.R. Imadi, A. Gul, V. Altay and M. Ozturk, 2019. 'Heavy metal stress and responses in plants. International Journal of Environmental Science and Technology. 16(3): 1807-1828.

Giannopolitis, C.N. and S.K. Ries, 1977. 'Superoxid dismutase: I. occurrence in higher plants. Plant Physiology 59: 309-314.

Goldson A, M. Lam, C.H. Scaman, S. Clemens, and A.Kermode, 2008. 'Screening of phenylalanine ammonialyase in plant tissues, and retention of activity during dehydration'. Journal of the Science of Food and Agriculture. 88:619–625.

Greive, C.M. and S.R. Grattan, 1983. 'Rapid assay for determination of water-soluble quaternary amino compounds'. Plant Soil 70: 303-307.

Gülmez, Ö, D.Tiryaki, Ö. Faruk Algur, M. Şengül Köseoğlu, and E. Gezgincioğlu, 2020. 'Reduction of phytotoxic effect of cadmium heavy metal by biomass of edible fungus, Armillaria tabescens'. Iranian Journal of Plant Physiology.10(3): 3265-3272.

Gupta M., N. Karmakar, S. Sasmal, S. Chowdhury and S. Biswas, 2016. 'Free radical scavenging activity of aqueous and alcoholic extracts of Glycyrrhiza glabra L. measured by ferric reducing antioxidant power (FRAP), ABTS bleaching assay (αTEAC), DPPH assay and peroxyl radical antioxidant assay'. Int. J. Pharm. Toxicol. 4:.235–240.

Hasanuzzaman, M., K. Nahar, M.M. Rohman, T.I. Anee, Y. Huang and M. Fujita,2018. 'Exogenous Silicon Protects Brassica napus Plants from Salinity-Induced Oxidative Stress Through the Modulation of AsA-GSH Pathway, Thiol-Dependent Antioxidant Enzymes and Glyoxalase Systems'. Gesunde Pflanz. 70: 185–194.

Hodson, M.J. and D.E. Evans, 2020. 'Aluminum–silicon interactions in higher plants: an update'. Journal of Experimental Botany. 71(21): 6719-6729

Hosseinzadeh H. and M. Nassiri-Asl, 2015. 'Pharmacological effects of Glycyrrhiza spp. and its bioactive constituents: update and review'. Phytother. Res. 29:.1868–1886.

Imadi, S.R.,S. Waseem, A.G. Kazi, M.M. Azooz and P. Ahmad, 2016. 'Aluminum toxicity in plants: An overview. In: Plant Metal Interaction; Ahmad, P., (Ed.), Elsevier: Amsterdam, The Netherlands, pp. 1–20.

Imtiaz, M., M.S. Rizwan, M.A. Mushtaq, M. Ashraf, S.M. Shahzad, B. Yousaf, D.A. Saeed, M. Rizwan, M.A. Nawaz, and S. Mehmood, 2016. 'Silicon occurrence, uptake, transport and mechanisms of heavy metals, minerals and salinity enhanced tolerance in plants with future prospects: A review'. J. Environ. Manage. 183: 521–529.

Jang, S.W., Y. Kim, A.L. Khan, C.I. Na and I.J. Lee, 2018. 'Exogenous short-term silicon application regulates macro-nutrients, endogenous phytohormones, and protein expression in Oryza sativa L'. BMC Plant Biol. 18: 4. https://doi.org/10.1186/s12870-017-1216-y.

Jitender G., 2011. 'Glycinebetaine and abiotic stress tolerance in plants'. Plant Signaling & Behavior. 6(11): 1746-1751.

Khan, E. and M. Gupta, 2018. 'Arsenic-silicon priming of rice (Oryza sativa L.) seeds influence mineral nutrient uptakeand biochemical responses through modulation of Lsi-1, Lsi-2, Lsi-6 and nutrient transporter genes'. Sci. Rep. 8, 10301. https://doi.org/10.1038/s41598-018-28712-3.

Kopittke, P.M., A. Gianoncelli, G. Kourousias,  K. Green and B.A. McKenna, 2017. 'Alleviation of Al toxicity by Si is Associated with the formation of Al–Si complexes in root tissues of sorghum'. Frontiers in Plant Science. 8. https://doi.org/10.3389/fpls.2017.02189.

Ma J.F., N. Yamaji and N. Mitani-Ueno, 2011. 'Transport of silicon from roots to panicles in plants (Review)'. Proc. Jpn. Acad., Ser. B Phys Biol Sci. 87(7): 377-85.

Morkunas, I., A. Wo´zniak, V. Mai, R. Ruci´nska-Sobkowiak and P. Jeandet, 2018. 'The role of heavy metals in plant response tobiotic stress'. Molecules, 23, 2320. https://doi.org/10.3390/molecules23092320.

Muneer, S., Y.G. Park, S. Kim and B.R. Jeong, 2017. 'Foliar or subirrigation silicon supply mitigates high temperature stress in strawberry by maintaining photosynthetic and stress-responsive proteins'. J. Plant Growth Regul. 36: 836–845.

Nakashima, K., H. Takasaki, J. Mizoi, K. Shinozaki and K. Yamaguchi-Shinozaki, 2012. 'NAC transcription factors in plant abiotic stress responses'. BBA-Gene Regul. Mech. 1819, 97–103.

Nasrollahi, V., A. Mirzaie-asl, L. Khodaei,and S. Jamalian, 2016. 'The effect of drought stress on the activity of antioxidant enzymes of Glycyrrhiza glabra'. J. Funct. Environ. Bot. 6:16–23.

Qian, L., B. Chen and M. Chen, 2016. 'Novel alleviation mechanisms of aluminum phytotoxicity via released biosilicon from rice straw-derived biochars'. Scientific Reports. 6:29346. https://doi.org/10.1038/srep29346.

Oloumi H. and N. Hassibi, 2011. 'Study the correlation between some climate parameters and the content of phenolic compounds in roots of Glycyrrhiza glabra'. J. Med. Plants Res. 5: 6011–6016.

Pirzadah, T. B., B. Malik, S. T. Salam, P. Ahmad Dar and S. Rashid, 2019. 'Impact of heavy metal stress on plants and the role of various defense elements'. Iranian Journal of Plant Physiology. 9(4): 2883-2900.

Rahman A., S. Lee, H.C. Ji, A.H. Kabir, C.S. Jones and K. Lee, 2018. 'Importance of mineral nutrition for mitigating aluminum toxicity in plants on acidic soils: current status and opportunities'. Int. J. Mol. Sci. 19, 3073.https://dx.doi.org/10.3390/ijms19103073.

Rasheed, R., M. Iqbal, M.A. Ashraf, I. Hussain, F. Shafiq, A. Yousaf and A. Zaheer, 2017. 'Glycine betaine counteracts the inhibitory effects of waterlogging on growth, photosynthetic pigments, oxidative defence system, nutrient composition, and fruit quality in tomato'. J. Hortic. Sci. Biotechnol.  93: 385–91.

Rezaei S., T. Nejad Sattari, M. Assadi, R.A. Khavari Nejad,  and I. Mehregan, 2017. 'Study of glycyrrhizic acid contents from Glycyrrhiza glabra populations in Iran and their relation with environmental factors. Biodiversitas 18: 212–220.

Robatjazi R., R. Roshandel and  S. Hooshmand Benefits of silicon nutrition on growth, physiological and phytochemical attributes of basil upon salinity stress'. International Journal of Horticultural Science and Technology. 7:37-50.

Saad-Allah, K.M. and I.M. Abdelsalam. 2020. 'Abiotic stress triggers mitochondrial defense system: A comprehensive review'. Iranian Journal of Plant Physiology10(3): 3195-3212.

Sadat Hosseini M., D. Samsampour, M. Ebrahimi, J. Abadia and M. Khanahmadi, 2018. 'Effect of drought stress on growth parameters, osmolyte contents, antioxidant enzymes and glycyrrhizin synthesis in licorice (Glycyrrhiza glabra L.) grown in the field'. Phytochemistry. 156: 124–134.

Sadat Hosseini M., D. Samsampour, M. Ebrahimi, J. Abadia, A. Sobhani Najafabadi, E. Igartua and M. Khanahmadi, 2020. 'Evaluation of glycyrrhizin contents in licorice (Glycyrrhiza glabra L.) under drought and soil salinity conditions using nutrient concentrations and biochemical traits as biomarkers'. Acta Physiologiae Plantarum. 42: 103. https://doi.org/10.1007/s11738-020-03090-4

Sagisaka, S., 1976. 'The occurrence of peroxide in a perennial plant, Populus gelrica'. Plant Physiol. 57: 308–309.

Shetty R., C.S. Nair Vidya, N.B. Prakash, A. Lux and M. Vaculík, 2020.  'Aluminum toxicity in plants and its possible mitigation in acid soils by biochar: A review', Science of the Total Environment. 765, 142744.  https://doi.org/10.1016/j.scitotenv.2020.142744.

Singh, D., and S.K. Chauhan, 2011. 'Organic acids of crop plants in aluminum
detoxification'. Curr. Sci. 100: 1109–1515.

Smirnov, O.E., A.M. Kosyan, O.I. Kosyk and N.Y. Taran, 2015. 'Response of phenolic metabolism induced by aluminum toxicity in Fagopyrum esculentum Moench. Plants. Ukr. Biochem. J. 87: 129–135.

Yan G., X. Fan, M. Peng, C. Yin, Z. Xiao and Y. Liang, 2020. 'Silicon Improves Rice Salinity Resistance by Alleviating Ionic Toxicity and Osmotic Constraint in an Organ-Specific Pattern. Front Plant Sci. 11:260.  https://doi.org/10.3389/fpls.2020.00260.

Yang, L. T., Y.P. Qi, H.X. Jiang and L.S. Chen, 2013. 'Roles of organic acid anion secretation in aluminum tolerance of higher plants'. BioMed. Res. Int.,173682. doi: 10.1155/2013/173682

Yildirima, E., M. Ekincia, M. Turanb, A. Dursuna, R. Kula and F. Parlakova, 2015. 'Roles of glycine betaine in mitigating deleterious effect of salt stress on lettuce (Lactuca sativa L.)'. Arch. Agron. Soil Sci., 61: 1673–1689

Zamani, G.R., J. Shaabani,  and A. Izanloo, 2017. 'Silicon effects on the growth and yield of chickpea under salinity stress. International Journal of Agriculture and Biology, 19 (6): 1475-1482.

Zhang Y., Y. Liang, X. Zhao, X. Jin, L. Hou, Y. Shi, and G. Ahammed, 2019.  'Silicon compensates phosphorus deficit-induced growth inhibition by improving photosynthetic capacity, antioxidant potential, and nutrient homeostasis in tomato. Agronomy. 9,733. https://doi.org/10.3390/agronomy9110733.

Zhang, W., Z. Xie, L. Wang, D. Lang and X. Zhang, 2017. 'Silicon alleviates salt and drought stress of Glycyrrhiza uralensis seedling by altering antioxidant metabolism and osmotic adjustment'. J. Plant Res. 130: 611–624.

Zhu, J. K., 2016. 'Abiotic stress signaling and responses in plants'. Cell 167:313–324.