Document Type : Original Article

Authors

1 Department of Horticultural Science, Faculty of Agriculture, University of Zanjan, Zanjan, Iran

2 Department of Horticultural Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Iran

3 Department of Agricultural, Forest and Food Sciences, University of Torino, Italy

Abstract

Purpose: Lycium barbarum berries can be a source of natural antioxidants for human food production. Research method: To increase the antioxidant activity of secondary metabolites in goji berry seedlings, we applied amino acid L-phenylalanine (Phe: 0.5, 1, and 1.5 mM), sodium selenate (Se: 0.25, 0.5, and 1 mg. L-1), and nitroxine biological fertilizer (170, 330, and 500 μL.L-1) at three levels. Distilled water was the control treatment. The experiment took place at the research farm of Ferdowsi University of Mashhad during 2021-2022. Findings: The results revealed that the treatments significantly affected goji berry plants regarding physiological and chemical attributes. Phenylalanine, selenium, and nitroxine substantially affected photosynthetic pigments, including chlorophyll and carotenoid, antioxidant, and catalase during the two years of foliar application. The results showed that phenylalanine with selenium increased the amounts of flavonoids, anthocyanins, and carbohydrates in goji berry plants. Applying phenylalanine alone had a positive, more potent effect on the amount of phenylalanine ammonia-lyase enzyme, which shows the impact of this substance on the phenylpropanoid pathway. Using it with nitroxine enhanced the phenol content and superoxide dismutase activity significantly. Research limitations: There was no limitation. Originality/Value: According to the results of this experiment, during the two years of 2021 and 2022, phenylalanine improved antioxidant enzyme activity and other traits significantly. Using phenylalanine and sodium selenate at low concentrations increased all antioxidant compounds and improved plant growth.

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Main Subjects

Abbas, S. M. (2012). Effects of low temperature and selenium application on growth and the physiological changes in sorghum seedlings. Journal of Stress Physiology and Biochemistry8(1), 268-286.
Abd El-Aal, F. S., Shaheen, A. M., Ahmed, A. A., & Mahmoud, A. R. (2010). Effect of foliar application of urea and amino acids mixtures as antioxidants on growth, yield and characteristics of squash. Research Journal of Agriculture and Biological Sciences6(5), 583-588.
Aebi, H. (1984). Catalase in vitro. In Methods in Enzymology, 121-126. Academic Press. https://doi.org/10.1016/S0076-6879(84)05016-3.
Aghdam, M. S., Moradi, M., Razavi, F., & Rabiei, V. (2019). Exogenous phenylalanine application promotes chilling tolerance in tomato fruits during cold storage by ensuring supply of NADPH for activation of ROS scavenging systems. Scientia Horticulturae246, 818-825. https://doi.org/10.1016/j.scienta.2018.11.074.
Akkad, R., Kharraz, E., Han, J., House, J. D., & Curtis, J. M. (2019). Characterisation of the volatile flavour compounds in low and high tannin faba beans (Vicia faba var. minor) grown in Alberta, Canada. Food Research International, 120, 285-294.
Chongping, H., Wenjie, H., & Junlin, L. (2022). Selenium-and nano-selenium-mediated cold-stress tolerance in crop plants. In Selenium and nano-selenium in environmental stress management and crop quality improvement (pp. 173-190). Cham: Springer International Publishing. https://doi.org/10.1007/978-3-031-070631-9.
Colla, G., Nardi, S., Cardarelli, M., Ertani, A., Lucini, L., Canaguier, R., & Rouphael, Y. (2015). Protein hydrolysates as biostimulants in horticulture. Scientia Horticulturae196, 28-38. https://doi.org/10.1016/j.scienta.2015.08.037.
Dahham, A. A. (2021). The effect of nitroxin application and drought stress on growth and yield of two Persian and Iraqi celery populations.  IOP Conference Series: Earth and Environmental Science (Vol. 735, No. 1, p. 012046). IOP Publishing. https://doi.org/10.1088/1755-1315/735/1/012046.
Edahiro, J. I., Nakamura, M., Seki, M., & Furusaki, S. (2005). Enhanced accumulation of anthocyanin in cultured strawberry cells by repetitive feeding of L-phenylalanine into the medium. Journal of Bioscience and Bioengineering99(1), 43-47. https://doi.org/10.1263/jbb.99.43.
El-Desouky, S. A., Ismaeil, F. H., Wanas, A. L., Fathy, E. S. L., Abd El-All, M. M., & Abd, M. M. (2011). Effect of yeast extract, amino acids and citric acid on physioanatomical aspects and productivity of tomato plants grown in late summer season. Minufiya Journal of Agricultural Research, 36(4), 859-884.
El-Ramady, H., Abdalla, N., Taha, H.S., Alshaal, T., El-Henawy, A., Faizy, S.E.D.A., Shams, M.S., Youssef, S.M., Shalaby, T., Bayoumi, Y., & Elhawat, N. (2016). Selenium and nano-selenium in plant nutrition. Environmental Chemistry Letters, 14, 123-147.
Fahramand, M., & Zohoori, M. (2013). Evaluate the effect biological fertilizer on some quantitative traits in maize. International Journal of Agriculture and Crop Sciences, 6(12), 789.
Garavand, F., Rahaee, S., Vahedikia, N., & Jafari, S. M. (2019). Different techniques for extraction and micro/nanoencapsulation of saffron bioactive ingredients. Trends in Food Science & Technology, 89, 26-44.
Garcia, A. L., Madrid, R., Gimeno, V., Rodriguez-Ortega, W. M., Nicolas, N., & Garcia-Sanchez, F. (2011). The effects of amino acids fertilization incorporated to the nutrient solution on mineral composition and growth in tomato seedlings. Spanish Journal of Agricultural Research9(3), 852-861. https://doi.org/10.5424/sjar/20110903-399-10.
Ghasemzadeh, A., Azarifar, M., Soroodi, O., & Jaafar, H. Z. (2012). Flavonoid compounds and their antioxidant activity in extract of some tropical plants. Journal of Medicinal Plants Research, 6(13), 2639-2643.
Giannopolitis, C. N., & Ries, S. K. (1977). Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology59(2), 309-314. https://doi.org/10.1104/pp.59.2.309.
Giglou, R. H., Giglou, M. T., Estaji, A., Bovand, F., & Ghorbanpour, M. (2023). Light-emitting diode irradiation and glycine differentially affect photosynthetic performance of black henbane (Hyoscyamus niger L.). South African Journal of Botany, 155, 230-240.‏
Gong, A., Wu, X., Qiu, Z., & He, Y. (2013). A handheld device for leaf area measurement. Computers and Electronics in Agriculture, 98, 74-80.‏
Hajiboland, R., Rahmat, S., Aliasgharzad, N., & Hartikainen, H. (2015). Selenium-induced enhancement in carbohydrate metabolism in nodulated alfalfa (Medicago sativa L.) as related to the glutathione redox state. Soil Science and Plant Nutrition61(4), 676-687. https://doi.org/10.1080/00380768.2015.1032181.
Hashem, A., Abd_Allah, E. F., Alqarawi, A. A., Al Huqail, A. A., Egamberdieva, D., & Wirth, S. (2016). Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi Journal of Biological Sciences23(2), 272-281. https://doi.org/10.1016/j.sjbs.2015.11.002.
Hatier, J. H. B., & Gould, K. S. (2008). Foliar anthocyanins as modulators of stress signals. Journal of Theoretical Biology, 253(3), 625-627.
Heydarnajad Giglou, R., & Torabi Giglou, M. (2023). Effects of calyx coating and storage temperature on antioxidant substances of Cape gooseberry (Physalis peruviana L.). International Journal of Horticultural Science and Technology, 10(1), 23-32.‏
Heydarnajad Giglou, R., Torabi Giglou, M., Hatami, M., & Ghorbanpour, M. (2024). Potential of natural stimulants and spirulina algae extracts on Cape gooseberry plant: A study on functional properties and enzymatic activity. Food Science & Nutrition, 12(11), 9056-9068. https://doi.org/10.1002/fsn3.4342
Huang, C., Qin, N., Sun, L., Yu, M., Hu, W., & Qi, Z. (2018). Selenium improves physiological parameters and alleviates oxidative stress in strawberry seedlings under low-temperature stress. International Journal of Molecular Sciences19(7), 1913. https://doi.org/10.3390/ijms19071913.
Jacobo-Velázquez, D. A., Martínez-Hernández, G. B., del C. Rodríguez, S., Cao, C. M., & Cisneros-Zevallos, L. (2011). Plants as biofactories: Physiological role of reactive oxygen species on the accumulation of phenolic antioxidants in carrot tissue under wounding and hyperoxia stress. Journal of Agricultural and Food Chemistry59(12), 6583-6593. https://doi.org/10.1021/jf2006529.
Jalil Sheshbahreh, M., Movahhedi Dehnavi, M., Salehi, A., & Bahreininejad, B. (2022). Nitroxin improves yield and phenol compound of purple coneflower (Echinaceae purpurea L.) root under different irrigation regimes. Journal of Organic Farming of Medicinal Plants1(1), 1-8.
Jiang, Y., Fang, Z., Leonard, W., & Zhang, P. (2021). Phenolic compounds in Lycium berry: composition, health benefits and industrial applications. Journal of Functional Foods77, 104340. https://doi.org/10.1016/j.jff.2020.104340.
Kaijv, M., Sheng, L., & Chao, C. (2006). Antioxidation of flavonoids of green rhizome. Food Science, 27(3), 110-115.
Kandil, E. E., Marie, E. A., & Marie, E. A. (2017). Response of some wheat cultivars to nano-, mineral fertilizers and amino acids foliar application. Alexandria science exchange journal38, 53-68. https://dx.doi.org/10.21608/asejaiqjsae.2017.1877.
Khaki, S., Wang, L., & Archontoulis, S. V. (2020). A CNN-RNN framework for crop yield prediction. Frontiers in Plant Science, 10, 1750.‏
Khan, S., Yu, H., Li, Q., Gao, Y., Sallam, B. N., Wang, H., ... & Jiang, W. (2019). Exogenous application of amino acids improves the growth and yield of lettuce by enhancing photosynthetic assimilation and nutrient availability. Agronomy9(5), 266. https://doi.org/10.3390/agronomy9050266.
Kovács, V., Gondor, O. K., Szalai, G., Darkó, É., Majláth, I., Janda, T., & Pál, M. (2014). Synthesis and role of salicylic acid in wheat varieties with different levels of cadmium tolerance. Journal of Hazardous Materials, 280, 12-19.
Krizek, D. T., Britz, S. J., & Mirecki, R. M. (1998). Inhibitory effects of ambient levels of solar UV‐A and UV‐B radiation on growth of cv. New Red Fire lettuce. Physiologia Plantarum103(1), 1-7. https://doi.org/10.1034/j.1399-3054.1998.1030101.x.
Liu, N., Shen, Y., & Huang, B. (2015). Osmoregulants involved in osmotic adjustment for differential drought tolerance in different bentgrass genotypes. Journal of the American Society for Horticultural Science140(6), 605-613. https://doi.org/10.21273/JASHS.140.6.605.
Mozafariyan, M., Shekari, L., Hawrylak-Nowak, B., & Kamelmanesh, M.M. (2014). Protective role of selenium on pepper exposed to cadmium stress during reproductive stage. Biological Trace Element Research, 160, 97–107.
Najafi, S., Nazari Nasi, H., Tuncturk, R., Tuncturk, M., Sayyed, R.Z., & Amirnia, R. (2021). Biofertilizer application enhances drought stress tolerance and alters the antioxidant enzymes in medicinal pumpkin (Cucurbita pepo convar. pepo var. Styriaca). Horticulturae, 7(12), 588.
Namvar, K., Salehi, E. A., & Mokhtarian, N. (2018). Total phenolic compounds and antioxidant activity of Stachys turomanicaJournal of Biosciences, 34(5), 1349-1356.
Oğuz, I., Oğuz, H.I., Vural, A.A., & Kafkas, N.E. (2022). Goji Berry (spp.) Cultivation in Turkey. In Proceedings of the Latvian Academy of Sciences. Section B. Natural, Exact, and Applied Sciences. 76(4):409-416
Ozkan, E. E., Ozden, T. Y., Toplan, G. G., & Mat, A. (2018). Phenolic content and biological activities of Lycium barbarum L (Solanaceae) fruits (Goji berries) cultivated in Konya, Turkey. Tropical Journal of Pharmaceutical Research, 17(10), 2047-2053. https://doi.org/10.4314/tjpr.v17i10.22.
Pakkish, Z. & Mohammadrezakhani, S., (2021). Quality characteristics and antioxidant activity of the mango (Mangifera indica) fruit under arginine treatment. Journal of Plant Physiology and Breeding, 11(1), 63-74.
Puccinelli, M., Malorgio, F., & Pezzarossa, B. (2017). Selenium enrichment of horticultural crops. Molecules, 22(6), 933. https://doi.org/10.3390/molecules22060933.
Qian, D., Zhao, Y., Yang, G., & Huang, L. (2017). Systematic review of chemical constituents in the genus Lycium (Solanaceae). Molecules, 22(6), 911.‏
Rady, M. M., Belal, H. E., Gadallah, F. M., & Semida, W. M. (2020). Selenium application in two methods promotes drought tolerance in Solanum lycopersicum plant by inducing the antioxidant defense system. Scientia Horticulturae, 266, 109290. https://doi.org/10.1016/j.scienta.2020.109290
Radyuk, M. S., Domanskaya, I. N., Shcherbakov, R. A., & Shalygo, N. V. (2009). Effect of low above-zero temperature on the content of low-molecular antioxidants and activities of antioxidant enzymes in green barley leaves. Russian Journal of Plant Physiology56, 175-180. https://doi.org/10.1134/S1021443709020058.
Rahi, A. R. (2013). Effect of nitroxin biofertilizer on morphological and physiological traits of Amaranthus retroflexus. Iranian Journal of Plant Physiology, 4(1), 899-905.
Ramos, S. J., Faquin, V., Guilherme, L. R. G., Castro, E. M., Ávila, F. W., Carvalho, G. S., ... & Oliveira, C. (2010). Selenium biofortification and antioxidant activity in lettuce plants fed with selenate and selenite. Plant, Soil and Environment, 56(12), 584–588.
Ríos, J.J., Blasco, B., Cervilla, L.M., Rosales, M.A., Sanchez‐Rodriguez, E., Romero, L., & Ruiz, J.M. (2009). Production and detoxification of H2O2 in lettuce plants exposed to selenium. Annals of Applied Biology, 154(1),107-116.
Sarojnee, D. Y., Navindra, B., & Chandrabose, S. (2009). Effect of naturally occurring amino acid stimulants on the growth and yield of hot peppers. Journal of Animal and Plant Sciences, 5(1), 414-424.
Simojoki, A., Xue, T., Lukkari, K., Pennanen, A., & Hartikainen, H. (2003). Allocation of added selenium in lettuce and its impact on roots. Agricultural and Food Science in Finland, 12(3-4), 155-164.
Shetta, N. D., & Zayed, M. Z. (2016). Responses of Acacia gerrardii and Vachellia origena Seedlings to mineral fertilization and salinity stress in Saudi Arabia. Alexandria Science Exchange Journal, 37, 430-439.
Shoaei, S., Noor-mohammadi, G., Choukan, R., Kashani, A., Heydari, S. H., & Rafiei, F. (2012). Study of nutrient accumulation in the aerial and forage yield affected by using of nitroxin, supernitro plus and biophosphor in order to reduce consumption of chemical fertilizers and drought-resistant in corn (KSC-704). Advances in Environmental Biology, 125-132.‏
Sogvar, O. B., Rabiei, V., Razavi, F., & Gohari, G. (2020). Phenylalanine alleviates postharvest chilling injury of plum fruit by modulating antioxidant system and enhancing the accumulation of phenolic compounds. Food Technology and Biotechnology58(4), 433-444. https://doi.org/10.17113/ftb.58.04.20.6717.
Teixeira, W. F., Fagan, E. B., Soares, L. H., Umburanas, R. C., Reichardt, K., & Neto, D. D. (2017). Foliar and seed application of amino acids affects the antioxidant metabolism of the soybean crop. Frontiers in Plant Science8, 327. https://doi.org/10.3389/fpls.2017.00327.
Turakainen, M., Hartikainen, H., & Seppänen, M. M. (2004). Effects of selenium treatments on potato (Solanum tuberosum L.) growth and concentrations of soluble sugars and starch. Journal of Agricultural and Food Chemistry, 52(17), 5378-5382. https://doi.org/10.1021/jf040077x.
Tzin, V., & Galili, G. (2010). New insights into the shikimate and aromatic amino acids biosynthesis pathways in plants. Molecular plant3(6), 956-972. https://doi.org/10.1093/mp/ssq048.
Ulianych, O., Yatsenko, V., Kondratenko, P., Lazariev, O., Voievoda, L., Lukianets, O., Adamenko, D. (2020). The influence of amino acids on the activity of antioxidant enzymes, malonic dialdehyde content and productivity of garlic (Allium sativum L.). Agronomy Research, 18(3), 2245-2258.
Wagner, G. J. (1979). Content and vacuole/extravacuole distribution of neutral sugars, free amino acids, and anthocyanin in protoplasts. Plant Physiology, 64(1), 88-93.
Wang, F., Sun, Y., & Shi, Z. (2019). Arbuscular mycorrhiza enhances biomass production and salt tolerance of sweet sorghum. Microorganisms7(9), 289.    https://doi.org/10.3390/microorganisms7090289.
Watanabe, S., Ohtani, Y., Tatsukami, Y., Aoki, W., Amemiya, T., Sukekiyo, Y., ... & Ueda, M. (2017). Folate biofortification in hydroponically cultivated spinach by the addition of phenylalanine. Journal of Agricultural and Food Chemistry, 65 (23), 4605-4610. https://doi.org/10.1021/acs.jafc.7b01375.
Weng, M., Cui, L., Liu, F., Zhang, M., Shan, L. & Yang, S. (2015). Effects of drought stress on antioxidant enzymes in seedlings of different wheat genotypes. Pakistan Journal of Botany, 47, 49–45.
Wu, F., Zhang, D., Zhang, H., Jiang, G., Su, X., Qu, H., ... & Duan, X. (2011). Physiological and biochemical response of harvested plum fruit to oxalic acid during ripening or shelf-life. Food Research International44(5), 1299-1305. https://doi.org/10.1016/j.foodres.2010.12.027.
Yossa Nzeuwa, I. B., Guo, B., Zhang, T., Wang, L., Ji, Q., Xia, H., & Sun, G. (2019). Comparative metabolic profiling of Lycium fruits (Lycium barbarum and Lycium chinense) from different areas in China and from Nepal. Journal of Food Quality, (1), 4396027.
Zahedyan, A., Jahromi, A. A., Zakerin, A., Abdossi, V., & Torkashvand, A. M. (2022). Nitroxin bio-fertilizer improves growth parameters, physiological and biochemical attributes of cantaloupe (Cucumis melo L.) under water stress conditions. Journal of the Saudi Society of Agricultural Sciences21(1), 8-20. https://doi.org/10.1016/j.jssas.2021.06.017.
Zhang, S., Hu, F., Li, H., & Li, X. (2009). Influence of earthworm mucus and amino acids on tomato seedling growth and cadmium accumulation. Environmental Pollution157(10), 2737-2742. https://doi.org/10.1016/j.envpol.2009.04.027.
Zhu, Z., Zhang, Y., Liu, J., Chen, Y., & Zhang, X. (2018). Exploring the effects of selenium treatment on the nutritional quality of tomato fruit. Food Chemistry252, 9-15. https://doi.org/10.1016/j.foodchem.2018.01.064.