Leaf chlorophyll content, phenolic content, flavonoid content and antioxidant activity of collard greens in response to fertilizer value of duckweed
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Abstract
Biennial collard greens (Brassica oleracea var acephala cv Morris Heading) are leafy vegetables that serve as an excellent source of phenolic and flavonoid compounds. Information concerning the supplementary effects of duckweed as a sole organic source of plant nutrition to enhance the content of certain phytochemicals in this vegetable remains limited. The research assessed the extent to which duckweed pellets and dried duckweed used as fertilizer affected the chlorophyll content of collard green leaves along with the total phenolic as well as flavonoid content and antioxidant properties of the vegetable. Assessments during consecutive dry and wet seasons were carried out from January to July 2022. The treatments comprised 330 kg of organically cultivated paddy soil (control), 300 kg of organically cultivated paddy soil supplemented with the sole dried duckweed, sole duckweed pellet and various ratios of dried duckweed (duckweed pellets). The combination of dried duckweed and duckweed pellet with organically cultivated paddy soil produced the maximum leaf chlorophyll content, greater antioxidant activity, and increased overall phenolic and flavonoid content compared to that recorded for the control in each of the seasons studied. The relationship between total phenolic content and antioxidant activity was found to be strongly positive according to Pearson correlation coefficient analysis, indicating that it contributes more antioxidant activity than total flavonoid content.
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References
Alhasan, A. S. and Al-Ameri, D. T. (2021). Effects of macronutrient fertilization on plant growth, essential oil content, and chemical composition in medicinal and aromatic plants grown under different environmental conditions: a review. Natural Volatiles and Essential Oils, 8:2588-2601.
Alizadeh, A., Khosnkhui, M., Javidnia, K., Firuzi, O., Tafazoli, E. and Khalighi, A. (2010). Effects of fertilizer on yield, essential oil composition, total phenolic content and antioxidant activity in Satureja hortensis L. (Lemiaceae) cultivated in Iran. Journal of Medicinal and Plants Research 4:33-40.
Amarowicz, R., Cwalina-Ambroziak, B., Janiak, M. A. and Bogucka, B. (2020). Effect of N fertilization on the content of phenolic compounds in Jerusalem artichoke (Helianthus tuberosus L.) tubers and their antioxidant capacity. Agronomy, 10:1215. https://doi10.3390/ agronomy10081215.
Barroso, M. R., Matins, N., Barros, L., Antonio, A. L., Rodrigues, A. A., Sousa, M. K., Santos-Buelga, C. and Ferreira, I. C. F. R. (2018). Assessment of the nitrogen fertilization effect on bioactive compounds of frozen fresh and dried samples of Stevia rebaudiana Bertoni. Food Chemistry, 243:208-213. https://doi.org/10.1016/ j.foodchem.2017.09.137.
Bendary, E., Francis, R. R., Ali, H. M. G., Sarwat, M. I. and El Hady, S. (2013). Antioxidant and structure-activity relationships (SARs) of some phenolic and anilines compounds. Annal of Agricultural Sciences, 58:173-781.
Bhuvana, P., Anuradha, V., Syed Ali, M., Suganya, V. and Sangeetha, P. (2018). Cultivation, phytochemical screening and quantitative analysis of phytocompounds in Chlorella vulgaris. Bioscience Discovery., 9:244.250.
Biesiada, A., Nawirska-Olszańska, A., Kucharska, A., Sokól-Letowska, A. and Kadra, K. (2010). The effect of nitrogen fertilization on nutritive value and antioxidative activity of red cabbage. Acta Scientiarum Polonorum Horturum Cultus, 9:13-21.
Bog, M., Sree, K. L., Fuchs, J., Hoang, P. T. N., Schubert, I., Kuever, J., Rabenstein, A., Paolacci, S., Jansen, M. A. K. and Appenroth, K. J. (2020). A taxonomic revision of Lemna sect. Uninerves (Lemnaceae). Taxon, 69:56-66.
Bojovic, B. and Stojanovic, J. (2005). Chlorophyll and carotenoid content in wheat cultivars as a function of mineral nutrition. Archives of Biological Sciences, 57:283-290.
Bray, R. H. and Kurtz, L. T. (1945). Determination of total organic and available forms of phosphorus in soils. Soil Sciences, 59:39-46.
Chrysargyris, A., Petropoulos, S. A., Fernandes, A., Barros, L., Tzortakis, N. and Ferreira, I.C.F.R. (2019). Effect of phosphorus application rate on Mentha spicata L. grown in deep flow technique (DFT). Food Chemistry, 276:84-92.
Chu, W., Zhengquan, W., Hailong, S. and Shenglei, G. (2006). Effects of different concentrations of nitrogen and phosphorus on chlorophyll biosynthesis, chlorophyll a fluorescence, and photosynthesis in Larix olgensis seedlings. Frontiers of Forestry in China, 1:170-175. https://doi.org/10.1007/s11461-006-0019-3.
Cristina, B. and Constantin, D. (2011). The effect of copper sulphate on the production of flavonoids in Digitalis lanata cell cultures. Farmacia, 59:113-118.
Daughtry, C. S. T., Walthall, C.L., Kim, M. S., Brown de Colstoun, E. and McMurtrey, J. E. (2000). Estimating corn leaf chlorophyll concentration from leaf and canopy reflectance. Remote Sensing of Environment, 74:229-239.
Dhaniaputri, R., Suwono, H., Amin, M. and Lukiati, B. (2021). Introduction to plant metabolism, secondary metabolites biosynthesis pathway, and in-silico molecular docking for determination of plant medicinal compounds: and overview. Advanced in Biological Sciences Research, 22:373-382.
Di Silvestro, R. A. and Cousind, R. J. (1984). Mediation of endotoxin-induced changes in zinc metabolism in rats. American Journal of Physiology, 247:36-41.
Ebrahimian, S., Pirzad, A., Jalilian, J. and Rahimi, A. (2021). The effect of micronutrients supplementation (Fe, Zn, B and Mn) on antioxidant activity of milk thistle (Silybum marianum L.) under rainfed condition. Journal of Medicinal Plants and By-products, 1:43-50.
Farhat, N., Elkhouni, A. and Zorrig, W. (2016). Effects of magnesium deficiency on photosynthesis and carbohydrate partitioning. Acta Physiologiae Plantarum, 38:145. doi:10.1007/s11738-016-2165-z.
Ferreira, V. B., Da Silva, T. T. C., Couto, S. R. M. and Srur, A. U. O. S. (2015). Total phenolic compounds and antioxidant activity of organic vegetables consumed in Brazil. Food and Nutrition Sciences, 6:798-804. doi:10.4236/fns.2015.69083.
Gong, Y., Sohn, H., Xue, L., Firestone, G. L. and Bjeldanes, L. F. (2006). 3, 3’-Diindolylmethane is a novel mitochondrial H(+)-ATP synthase inhibitor that can induce p21(Cip1/Waf1) expression by induction of oxidative stress in human breast cancer cells. Cancer Research, 66:4880-4887.
Hanif, M. A., Nawaz, H., Ayub, M. A., Tabassum, N., Kanwal, N., Rashid, N., Saleem, M. and Ahmad, M. (2017). Evaluation of the effects of zinc on the chemical composition and biological activity of basil essential oil by using Raman spectroscopy. Industrial Crops and Products, 96:91-101. https://doi.org/10.1016/j.indcrop.2016.10.058.
Hanlon, E. A. (1998). Elemental determination by atomic absorption spectrophotometry. In: Handbook of reference methods for plant analysis, Boca Raton, Florida, CRC Press. pp.157-164.
Hussein, M. M., El-Faham, S. Y. and Alva, A. K. (2012). Pepper plants growth, yield, photosynthetic pigments, and total phenols as affected by foliar application of potassium under different salinity irrigation water. Agricultural Science, 3:241-248.
Ibrahim, M. H., Hawa, Z. E., Jaafar, H. Z., Karimi, E. and Ghasemzadeh, A. (2013). Impact of organic and inorganic fertilizers application on the phytochemical and antioxidant activity of Kacip Fatimah (Labisia pumila Benth). Molecules, 18:10973-10988. https://doi.org/10.3390/molecules180910973.
Jilimane, K. (2019). Nitrogen and phosphorus release in soil and fertilizer value of Lemna minor biomass relative to chicken litter compost. (Master Thesis). University of KwaZulu-Natal, Pietermaritzburg.
Joel, O. O., Nawiri, P., Musila, W. and Gweyi-Onyango, J. P. (2017). Effect of phosphorus deficiency on phenolics and antioxidants content of two African nightshade varieties grown in Kenya. International Journal of Plant & Soil Science, 15:1-11.
Journey, W. K., Skillicorn, P. and Spira, W. (1993). Duckweed Aquaculture: A New Aquatic Farming System for Developing Countries. The world Bank. p. 69.
Kaewnarin, K., Niamsup, H., Shank, L. and Rakariyatham, N. (2014). Antioxidant and antiglycation activities of some edible and medicinal plants. Chiang Mai Journal of Science, 41:105-116.
Kasinath, B. L., Senthivel, T. and Ganeshmurthy, A. N. (2014). Effect of magnesium application on chlorophyll content and yield of tomato. Plant Archives, 142:801-804.
Khathutshelo, M. V., Mpumelelo, N., Wonder, N. and Fhatuwani, M. N. (2016). Effects of foliar spray application of selected micronutrients on the quality of bush tea. HorTScience., 51:873-879.
Kopsell, D. A., Kopsell, D. E. and Curran-Celentano, J. (2007). Carotenoid pigments in kale are influenced by nitrogen concentration and form. Journal of the Science of Food and Agriculture, 87:900-907.
Land Development Department. (2010). Manual of soil chemical analysis procedure. Retrieved from http://www.ldd.go.th/PMQA/2553/Manual/OSD-03.pdf.
Landolt, E. and Kandeler, R. (1987). Biosystematic investigations on the family of duckweeds (Lemnaceae). Vol. 4, Published in the Geobotanischen Instituties der ETH, Stiftung Rubel Zurich. 638p.
Larcher, W. (1995). Physiological plant ecology. In: Ecophysiology and Stress Physiology of Functional Groups (3rd ed.). Springer, New York: 528p.
LECO Corporation (2018). Operation In: Trumac 828 series carbon/nitrogen analyzer instruction manual. LECO Europe B.V., U.S., pp.3-48.
Li, J., Zhu, Z. and Gerandas, J. (2008). Effects of nitrogen and sulfur on total phenolics and antioxidant activity in two genotypes of leaf mustards. Journal of Plant Nutrition, 31:1642-1655. https://doi.org/10.1080/01904160802244860.
Li, M., Paré, P. W., Zhang, J., Kang, T., Zhang, Z., Yang, D., Wank, K. and Xing, H. (2018). Antioxidant capacity connection with phenolic and flavonoid content in chinese medicinal herbs. Records of Natural Products, 12:239-250.
Lindsay, W. L. and Norvell, W. A. (1978). Development of a DTPA soil test for zinc, iron, manganese and copper. Soil Science Society of America Journal, 42:421-128.
Lu, Z., Lu, J., Pan, Y., Lu, P., Li, X., Cong, R. and Ren, T. (2016). Anatomical variation of mesophyll conductance under potassium deficiency has a vital role in determining leaf photosynthesis: structural controls on gm under K deficiency. Plant, Cell & Environment, 39:2428-2439.
Mudau, F. N., Soundy, P. and du Toit, E. S. (2007). Effects of nitrogen, phosphorus and potassium nutrition on total polyphenol content of bush tea (Athrixia phylicoides L.) leaves in shaded nursery environment. HorTScience., 42:334-338.
Muflihah, Y. M., Gollavelli, G. and Ling, Y. C. (2021). Correlation study of antioxidant activity with phenolic and flavonoid compounds in 12 Indonesian indigenous herbs. Antioxidants, 10:1530. https://doi.org/10.3390/antiox10101530.
Nagaveni, H. C., Kumari, C. B. C. and Suma, A. M. (2018). Effect of different nutrient levels on growth and yield of some medicinal plants. Journal of Pharmacognosy and Phytochemistry, 7:10-113.
Panche, A. N., Diwan, A. D. and Chandra, S. R. (2016). Flavonoids: An overview. J. Nutr. Sci. 5:e47. doi:10.1017/jns.2016.41.PMID:28620474; PMCID:PMC5465813.
Pandey, V., Patel, A. and Patra, D. D. (2015). Amelioration of mineral nutrition, productivity, antioxidant activity and aroma profile in marigold (Tagetes minuta L.) with organic and chemical fertilization. Industrial Crops and Products, 76:378-385. https://dx.doi.org/ 10.1016/j.indcrop.2015.07.023.
Panhwar, Q. A., Naher, U. A., Radziah, O., Shamshuddin, J., Mohd Razi, I., Dipti, S. S. and Karabalei Aghamolki, M.T. (2015). Quality and antioxidant activity of rice grown on alluvial soil amended with Zn, Cu and Mo. South African Journal of Botany, 98:77-83. https://dx.org/10.1016/ j.sajb.2015.01.021.
Powell, S. R. (2000). The antioxidant properties of zinc. Journal of Nutrition, 130:1447s-1454s.
Purbajanti, E. D., Slamet, W., Fuskhah, E. and Rosyida. (2019). Effects of organic and inorganic fertilizers on growth, activity of nitrate reductase and chlorophyll contents of peanuts (Arachis hypogaea L.). IOP Conference Series Earth and Environtal Science, 250.012048. doi:10.1.1088/1755-1315/250/1/102048.
Saeed, N., Khan, M. R. and Shabbir, M. (2012). Antioxidant activity, total phenolic and total flavonoid contents of whole plant extracts Torilis leptophylla L. BMC Complementary and Alternative Medicine, 12:221. https://doi.org/10.1186/1472-6882-12-221.
Salehi, A., Fallah, S., Kaul, H. P. and Zitterl-Eglseer, K. (2018). Antioxidant capacity and polyphenols in buckwheat seeds from fenugreek/buckwheat intercrops as influenced by fertilization. Journal of Cereal Science, 84:142-150.
Saltveit, M. E. (2010). Synthesis and metabolism of phenolic compounds. In: Fruit and Vegetable phytochemicals; chemistry, nutritional value and stability, Publisher: Wiley-Blackwell. pp.89-100.
Sharafzadeh, S. (2011). Effect of nitrogen, phosphorus and potassium on growth, essential oil and total phenolic content of garden thyme (Thymus vulgaris L.). Advances in Environmental Biology, 5:699-703.
Siwasin, N. (1984). Methods of analysis for soils and plants. Department of Soil Science and Conservative Science, Chiangmai University, Thailand, pp.138.
Skwarylo-Bednarz, B. and Krzepilko, A. (2009). Effect of various doses of N P K fertilizers on chlorophyll content in the leaves of two varieties of amaranth (Amaranthus cruentus L.). Ecological Chemistry and Engineering S, 16:1373-1377.
Stephens, J. M. (1994). Collards – Brassica oleracea L. (Acephala group). UF/IFAS Extension. https://edis.ifas.ufl.edu/publication/MV053.
Suwanawong, S. (2001). Analysis of plant nutrition. Bangkok, Kasetsart University Press, Thailand. p. 141.
Theerachindakhajorn, P. (2011). Handbook of soil chemical analysis. Khon Kaen, Khon Kaen University Press, Thailand. p. 174.
Treutter, D. (2010). Managing phenol contents in crop plants by phytochemical farming and breeding-visions and constraints. International Journal of Molecular Science, 11: 807-857. https://doi.org/ 10.3390/ijms11030807.
Tränkner, M., Tavakol, E. and Jákli, B. (2018). Functioning of potassium and magnesium in photosynthesis, photosynthate translocation and photoprotection. Physiologia Plantarum, 163:414-431.
Uysal, E. (2018). Effects of nitrogen fertilization on the chlorophyll content of apple. Meyve Bilimi/Fruit Science, 5:12-17.
Vetrano, F., Miceli, A., Moncada, A., Mustazza, G. and Romano, C. (2013). Collard green (Brassica oleracea var. acephala) cultivation in Sicily. Acta Horticulturae, 1005:471-477. https://doi.org/10.17660/AactaHortic.2013.1005.57.
Vinha, A. F., Barreira, S. V. P., Costa, A. S. G., Alves, R. C. and Oliveira, M. B. P. P. (2014). Organic versus conventional tomatoes: Influence on physicochemical parameters, bioactive compounds and sensorial attributes. Food and Chemical Toxicology, 67:139-144. https://doi.org/10.1016/j.fct.2014.02.018.
Walkley, A. and Black, I. A. (1947). Chromic acid titration method for determination of soil organic matter. Soil Science Society of America Proceedings, 63:257.
Wang, F., Liu, P. and Zhu, J. W. (2004). Effect of magnesium (Mg) on root activity, chlorophyll content and membrane permeability of soybean. Journal of Agro-Environment Science, 23:235-239.
Yingngam, B., Monschein, M. and Brantner, A. (2014). Ultrasound-assited extraction of phenolic compounds from Cratoxylum formosum ssp. formosum leaves using central composite design and evaluation of its protective ability against H2O2-induced cell death. Asian Pacific Journal of Tropical Medicine, 7:5497-5505.
Zhao, C., Wang, Z., Cui, R., Su, L., Sun, X., Li, O., Borras-Hidalgo, K., Wei, J., Yue, Q. and Zhao, L. (2021). Effects of nitrogen application on phytochemical component levels and anticancer and antioxidant activities of Allium fistulosum. PeerJ., 9:e11706.http://doi.org/107717/peerj.11706.
Zhao, D., Oosterhuis, D. M. and Bednarz, C. W. (2001). Influence of potassium deficiency on photosynthesis, chlorophyll content, and chloroplast ultrastructure of cotton plants. Photosynthetica, 39:103-109.
Zhao, X., Nechols, J. R., Williams, K., Wangc, W. and Carey, E. E. (2009). Comparison of phenolic acids in organically and conventionally grown pac choi (Brassica rapa L. chinensis). Journal of the Science of Food and Agriculture,89:940-946. https://doi.org/10.1002/jsfa.3534.
Zheng, C., Huang, Y. X. and Liu, K. X. (2019). Influence of magnesium on photosynthetic characteristics and growth effects of sugarcane at seedling stage. American Journal of Biochemistry and Biotechnology, 15:33-38.
Ziegler, P., Adelmann, K., Zimmer, S., Schmidt, C. and Appenroth, K. J. (2015). Relative in vitro growth rates of duckweeds (Lemnaceae) the most rapidly growing higher plants. Plant Biology, 17:33-41.
