The effects of glycine betaine and L-arginine on biochemical properties of pot marigold (calendula officinalis L.) under water stress

Document Type : Original Article

Authors

1 Department of Horticulture and Agronomy Science, Islamic Azad University, Science and Research branch, Tehran, Iran

2 Department of Horticulture, Faculty of Agriculture, Islamic Azad University, Saveh Branch, Saveh, Iran

3 Plant Biotechnology Group, National Institute of Genetic Engineering and Biotechnology (NIGEB), Tehran, Iran

10.22034/ijpp.2019.667133

Abstract

Pot marigold (Calendula officinalis L.) is widely used due to its various biological activities to treat diseases as an analgesic, anti-diabetic, anti-ulcer and anti-inflammatory agent. To ameliorate the adverse effects of water stress on this medicinal plant, foliar application of glycine betaine (GB) and L-arginine (LA) was used. For this purpose, water stress was applied at three levels (100%, 70% , and 40% field capacity (FC)), and foliar application was used at five levels (control, 50 mM GB, 100 mM GB, 1.5 mM LA, and 3 mM LA) as factorial based on completely randomized  design. We measured phenol and flavonoid content, DPPH radical scavenging activity, superoxide dismutase (SOD) and phenylalanine ammonia-lyase (PAL) activity, and essential oil (EO) content and yield. Total phenol content in the interaction of 40% FC and GB 100 mM was higher than the other treatments. The highest and lowest total flavonoid content and DPPH radical scavenging activity were observed in the interaction of 40% FC and 100% FC, respectively. These variables at GB 100 mM were greater than the others. The highest SOD and PAL activity was found in the interaction of 40% FC and LA 3 mM/GB 100 mM. The content and yield of EO in the interaction of 70% FC and 100 mM GB were greater than other treatments. In sum, 70% of water stress did not significantly change the biochemical properties of C. officinalis, but 40% FC dramatically influenced the quality of the plant. GB 100 mM could stimulate the plant to activate its antioxidant systems under water stress and obtain the highest EO.

Keywords


 

 

Aldred, E. M. 2008. 'Pharmacology E-Book: A Handbook for Complementary Healthcare Professionals'. Elsevier Health Sciences.
Ali, Q., M. Ashraf and F. Anwar. 2010. 'Seed composition and seed oil antioxidant activity of maize under water stress'. Journal of the American Oil Chemists' Society, 87(10): 1179-1187.
Ansari, W. A., N. Atri, B. Singh, P. Kumar, and S. Pandey. 2018. Morpho-physiological and biochemical responses of muskmelon genotypes to different degree of water deficit. Photosynthetica, 56(4), 1019-1030.
Ashraf, M. F., and M. Foolad. 2007. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and experimental botany, 59(2): 206-216.
Bausenwein, U., P. Millard and J. A. Raven. 2001. Remobilized old‐leaf nitrogen predominates for spring growth in two temperate grasses. New Phytologist, 152(2): 283-290.
Bettaieb, I., I. H. Sellami, S. Bourgou, F. Limam, and B. Marzouk. 2011. 'Drought effects on polyphenol composition and antioxidant activities in aerial parts of Salvia officinalis L. Acta Physiologiae Plantarum, 33: 1103–1111.
Bray, E. A. 2000.'Response to abiotic stress'. Biochemistry and molecular biology of plants, 1158-1203.
Bujor, O. C., C. Ginies, V. I. Popa, and C. Dufour. 2018. 'Phenolic compounds and antioxidant activity of lingonberry (Vacciniumvitis idaea L.) leaf, stem and fruit at different harvest periods'. Food chemistry, 252, 356-365.
Caser, M., F. D'Angiolillo, W. Chitarra, C. Lovisolo, B. Ruffoni, L. Pistelli, L., and V. Scariot. 2016. 'Water deficit regimes trigger changes in valuable physiological and phytochemical parameters in Helichrysum petiolare Hilliard & BL Burtt. Industrial Crops and Products, 83: 680-692.
Chen, C. N., and S. M. Pan. 1996. 'Assay of superoxide dismutase activity by combining electrophoresis and densitometry'. Bot. Bull. Acad. Sin. 37: 107-111
Chen, T. H., and N. Murata. 2011. 'Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications'. Plant, cell & environment, 34(1): 1-20.
Cunhua, S., S. Jian-jie, W. Dan, L. I. Bai-wei, and S. U. N. Dong. 2011. 'Effects on physiological and biochemical characteristics of medicinal plant pigweed by drought stresses'. Journal of Medicinal Plants Research, 5(17): 4041-4048.
Fan, C. H., B. Du, Y. C.  Zhang, Y. L. Gao and M. Chang. 2016. 'Determination of Lead and Cadmium in Calendula Officinalis Seedlings for Phytoremediation of Multi-Contaminated Loess by Using Flame Atomic Absorption Spectrometry with Wet Digestion'. Guangpuxueyuguangpu fen xi= Guangpu, 36(8), 2625-2628.
Fang, Y. and L. Xiong. 2015.' General mechanisms of drought response and their application in drought resistance improvement in plants'. Cellular and Molecular Life Sciences, 72(4): 673-689.
Fischer, S., R. Wilckens, J. Jara, J. and M. Aranda. 2013. 'Controlled water stress to improve functional and nutritional quality in quinoa seed'. BoletinLatinoamericano y del Caribe de Plantas Medicinales y Aromaticas, 12(5): 457–468.
Ganesan, D., E. Al-Sayed, A. Albert, E. Paul, A. N. B. Singab, S. GovindanSadasivam, and L. Saso. 2018. 'Antioxidant activity of phenolic compounds from extracts of Eucalyptus globulus and Melaleuca styphelioides and their protective role on D-glucose-induced hyperglycemic stress and oxalate stress in NRK-49F cells. Natural product research, 32(11), 1274-1280.
Geneva, M. P., I. V. Stancheva, M. M. Boychinova, N. H. Mincheva, and P. A. Yonova. 2010. 'Effects of foliar fertilization and arbuscular mycorrhizal colonization on Salvia officinalis L. growth, antioxidant capacity, and essential oil composition. Journal of the Science of Food and Agriculture, 90(4): 696-702.
Gharibi, S., B. E. S. Tabatabaei, G. Saeidi, and S. A. H. Goli. 2016. 'Effect of drought stress on total phenolic, lipid peroxidation, and antioxidant activity of Achillea species'. Applied biochemistry and biotechnology, 178(4): 796-809.
Hahlbrock, K. and H. Ragg.  1975. 'Light-induced changes of enzyme activities in parsley cell suspension cultures: effects of inhibitors of RNA and protein synthesis'. Archives of Biochemistry and Biophysics, 166(1): 41-46.
Hristozkova, M., M. Geneva, I. Stancheva, M., Boychinova, and E. Djonova. 2016. 'Contribution of arbuscular mycorrhizal fungi in attenuation of heavy metal impact on Calendula officinalis development'. Applied soil ecology, 101, 57-63.
Khalid, K. A. and J. A. T. da Silva. 2010. 'Yield, essential oil and pigment content of Calendula officinalis L. flower heads cultivated under salt stress conditions'. Scientia horticulturae, 126(2): 297-305.
Khorasaninejad, S., A. Mousavi, H. Soltanloo, K. Hemmati, and A. Khalighi. 2011. 'The effect of drought stress on growth parameters, essential oil yield and constituent of Peppermint (Mentha piperita L.)'. Journal of Medicinal Plants Research, 5(22): 5360-5365.
Kim, J. M., T. Sasaki, M. Ueda, K. Sako and M. Seki, M. 2015. 'Chromatin changes in response to drought, salinity, heat, and cold stresses in plants'. Frontiers in plant science, 6, 114.
Krol, A., R. Amarowicz, and S. Weidner. 2014. 'Changes in the composition of phenolic compounds and antioxidant properties of grapevine roots and leaves (Vitis vinifera L.) under continuous of long-term drought stress'. Acta Physiology Plant, 36: 1491–1499.
Kurepin, L. V. A. G. Ivanov, M.  Zaman, R. P.  Pharis, S. I. Allakhverdiev, V.  Hurry, V. and N. P. Hüner. 2015. 'Stress-related hormones and glycinebetaine interplay in protection of photosynthesis under abiotic stress conditions'. Photosynthesis research, 126(2-3): 221-235.
Lin, K. H., P. Y. Chao, C. M. Yang, W. C. Cheng, H. F. Lo and T. R. Chang. 2006. 'The effects of flooding and drought stresses on the antioxidant constituents in sweet potato leaves'. Botanical Studies, 47: 417–426.
Liu, H., X. Wang, D. Wang, Z. Zou, Z. and Z. Liang. 2011. 'Effect of drought stress on growth and accumulation of active constituents in Salvia miltiorrhiza Bunge'. Industrial Crops and Products, 33(1), 84-88.
Mansour, M. M. F. 2000. 'Nitrogen containing compounds and adaptation of plants to salinity stress'. Biologia Plantarum, 43(4): 491-500.
Mbarki, S., O. Sytar, A. Cerda, M. Zivcak, A. Rastogi, X. He, and M. Brestic. 2018. 'Strategies to Mitigate the Salt Stress Effects on Photosynthetic Apparatus and Productivity of Crop Plants'. In Salinity Responses and Tolerance in Plants, Volume 1 (pp. 85-136). Springer, Cham.
Metwally, S. A., K. A. Khalid and B. H. Abou-Leila. 2013. 'Effect of water regime on the growth, flower yield, essential oil and proline contents of Calendula officinalis'. Nusantara Bioscience, 5(2); 63-67.
Mohanty, A., H. Kathuria, A. Ferjani, A. Sakamoto, P. Mohanty, N. Murata, and A. Tyagi. 2002. 'Transgenics of an elite indica rice variety Pusa Basmati 1 harbouring the codA gene are highly tolerant to salt stress'. Theoretical and Applied Genetics, 106(1): 51-57.
Muley, B. P., S. S. Khadabadi and N. B. Banarase. 2009. 'Phytochemical constituents and pharmacological activities of Calendula officinalis Linn (Asteraceae): a review'. Tropical Journal of Pharmaceutical Research, 8(5): 23-31.
Nordin, A. and T. Näsholm. 1997. 'Nitrogen storage forms in nine boreal understorey plant species'. Oecologia, 110(4): 487-492.
Pan, Y., L. J. Wu, and Z. L. Yu. 2006. 'Effect of salt and drought stress on antioxidant enzymes activities and SOD isoenzymes of liquorice (Glycyrrhiza uralensis Fisch).' Plant Growth Regulation, 49(2-3): 157-165.
Pintea, A., C. Bele, S. Andrei and C. Socaciu. 2003. 'HPLC analysis of carotenoids in four varieties of Calendula officinalis L. flowers'. Acta Biologica Szegediensis, 47(1-4): 37-40.
Rahmani, N., J. Daneshian, H. A. Farahani, and T. Taherkhani. 2011.' Evaluation of nitrogenous fertilizer influence on oil variations of Calendula (Calendula officinalis L.) under drought stress conditions'. Journal of Medicinal Plants Research, 5(5): 696-701.
Rasheed, R., M. Iqbal, M. A. Ashraf, I. Hussain, F. Shafiq, A.Yousaf, and A. Zaheer. 2018. 'Glycine betaine counteracts the inhibitory effects of waterlogging on growth, photosynthetic pigments, oxidative defense system, nutrient composition, and fruit quality in tomato'. The Journal of Horticultural Science and Biotechnology, 93(4), 385-391.
Razmjoo, K. H., P. A. Heydarizadeh, and M. R. Sabzalian. 2008. 'Effect of salinity and drought stresses on growth parameters and essential oil content of Matricaria chamomile'. International journal of agriculture and biotechnology, 10(4): 451-454.
Reddy, A. R., K. V. Chaitanya, and M. Vivekanandan. 2004. 'Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants'. Journal of plant physiology, 161(11), 1189-1202.
Rennenberg, H., H. Wildhagen, and B. Ehlting. 2010. 'Nitrogen nutrition of poplar trees'. Plant Biology, 12(2): 275-291.
Rhodes, D. and A. D. Hanson. 1993.' Quaternary ammonium and tertiary sulfonium compounds in higher plants'. Annual review of plant biology, 44(1): 357-384.
Roy, M., and R. Wu. 2001. 'Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice'. Plant Science, 160(5): 869-875.
Sak, K., T. H. Nguyen, V. D.  Ho, T. T. Do, and A. Raal. 2017. 'Cytotoxic effect of chamomile (Matricaria recutita) and marigold (Calendula officinalis) extracts on human melanoma SK-MEL-2 and epidermoid carcinoma KB cells'. Cogent Medicine, 4(1), 1333218.
Sangwan, N. S., A. H. Farooqi, F. Shabih and R. S. Sangwan. 2001. 'Regulation of essential oil production in plants'. Plant growth regulation, 34(1): 3-21.
Schwinn, K. E., and K. M. Davies, 2018. 'Flavonoids'. Annual Plant Reviews, 92-149.
Shehab, G. G., O. K. AHMED, and H. S. El-Beltagi. 2010. 'Effects of various chemical agents for alleviation of drought stress in rice plants (Oryza sativa L.)'. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 38(1): 139-148.
Slinkard, K. and V. L. Singleton. 1977. 'Total phenol analysis: automation and comparison with manual methods'. American journal of enology and viticulture, 28(1): 49-55.
Subbarao, G. V., R. M. Wheeler, L. H. Levine, and G. W.  Stutte. 2001. 'Glycine betaine accumulation, ionic and water relations of red-beet at contrasting levels of sodium supply'. Journal of Plant Physiology, 158(6): 767-776.
Ukiya, M., T. Akihisa, K. Yasukawa, H. Tokuda, T. Suzuki, and Y. Kimura. 2006. 'Anti-inflammatory, anti-tumor-promoting, and cytotoxic activities of constituents of marigold (Calendula officinalis) flowers'. Journal of Natural Products, 69(12): 1692-1696.
Weidner, S., r. Amarowicz, M. Karamać, and E. Frączek, 2000. 'Changes in endogenous phenolic acids during development of Secalecereale caryopses and after dehydration treatment of unripe rye grains'. Plant Physiology and Biochemistry, 38(7-8): 595-602.
Xie, W., Z. Hao, X. Zhou, X. Jiang, X., L. Xu, S. Wu, and B. Chen. 2018. 'Arbuscular mycorrhiza facilitates the accumulation of glycyrrhizin and liquiritin in Glycyrrhiza uralensis under drought stress'. Mycorrhiza, 28(3): 285-300.
Yang, W. J., P. J. Rich, J. D. Axtell, K. V. Wood, C. C. Bonham, G. Ejeta, and D. Rhodes. 2003. 'Genotypic variation for glycinebetaine in sorghum'. Crop Science, 43(1): 162-169.
Yang, X. and C. Lu. 2005. 'Photosynthesis is improved by exogenous glycinebetaine in salt‐stressed maize plants'. Physiologia Plantarum, 124(3): 343-352.
Zainol, M. K., A. Abd-Hamid, S. Yusof, and R. Muse. 2003.' Antioxidative activity and total phenolic compounds of leaf, root and petiole of four accessions of Centella asiatica (L.) Urban'. Food Chemistry, 81, 575–581.
Zhishen, J., T. Mengcheng, and W. Jianming. 1999. 'The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals'. Food Chemistry, 64(4): 555-559.