Influence of fertilizer and salicylic acid treatments on growth, physiological, and antioxidant characteristics in green and red Perilla frutescens varieties
Perilla is herbaceous plant, functional food, and nutraceutical product with antioxidant properties. The objective of this study was to investigate the growth, reflectance indices, and antioxidant properties of P. frutescens species in response to fertilizer and salicylic acid (SA) applications. Two independent experiments were carried out in an environmentally controlled greenhouse: (1) pots of red-leaf and green-leaf cultivars divided into four groups treated with 10-30-20 (10N-13.1P-16.6K), 15-10-30 (15N-4.4P-24.9K), 20-20-20 (20N-8.7P-16.6K), and 30-10-10 (30N-4.4P-8.3K) fertilizers for periods of 10 weeks, and (2) pots of red and green Perilla cultivars divided into five groups treated with 0 (control), 125, 250, 500, and 1,000 µM of SA for periods of 7 weeks. Wide variations occurred in the agronomic performance, soil-plant analysis development (SPAD) value, adjusted normalized difference vegetation index (NDVI), maximal quantum yield of PSII photochemistry (Fv/Fm), and antioxidant activity of the two Perilla varieties. All the measured traits were higher in green than in red Perilla under identical fertilizing, and all agronomic traits in green and red Perilla plants subjected to 125 and 500 μM SA were better than in controls. The SPAD and NDVI values of all plants increased as N% increased, the lowest Fv/Fm values of all plants were observed under 15-10-30 fertilizer treatment, the lowest NDVI values were detected in controls, and the Fv/Fm values of all plants decreased under 1,000 μM SA treatment. These indices can be used as indicators to characterize the physiology of these plants and are suitable for evaluating their growth and development under specific fertilizer and SA treatments. Green Perilla leaf extract (PLE) contained higher rosmarinic acid (RA) concentration in each fertilizer treatment, and higher total phenolic (TP) and RA concentration in each SA treatment. However, red PLE contained higher caffeic acid (CA) concentration than green PLE in each fertilizer and SA treatment, implying that their two genotypes exhibited different abilities and specificities of photosynthetic metabolites, and that different varieties may prepare for 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging activity by up-regulating TP, RA, and CA concentration differently. Thus, Perilla plants can be used as health foods due to high TP, RA, and CA concentration. To produce Perilla efficiently in industrial applications, we undertook to determine the optimum N-P-K fertilizer ratio and SA application for maximizing the growth and accumulation of TP, RA, and CA in Perilla plants.
Ballester C, Zarco-Tejada PJ, Nicola E, Alarco JJ, Fereres E, Intrigliolo D, Gonzalez-Dugo V (2018). Evaluating the performance of xanthophyll, chlorophyll, and structure-sensitive spectral indices to detect water stress in five fruit tree species. Precision Agriculture 19:178-193. https://doi.org/10.1007/s11119-017-9512-y
Bajwa S, Mishra A, Norman R (2010). Canopy reflectance response to plant nitrogen accumulation in rice. Precision Agriculture 11:488-506. https://doi.org/10.1007%2Fs11119-009-9142-0
Beta T, Nam S, Dexter J, Sapirstein H (2017). Phenolic content and antioxidant activity of pearled wheat and roller-milled fractions. LWT-Food Science Technology 78:151-159. https://doi.org/10.1094/CC-82-0390
Boatwright JL, Karolina PM (2013). Salicylic acid: An old hormone up to new tricks. Molecular Plant Pathology 14:623-634. https://doi.org/10.1111/mpp.12035
Bonneville M, Fyles J (2006). Assessing variations in SPAD-502 Chlorophyll meter measurements and their relationships with nutrient content of trembling aspen foliage. Communications in Soil Science and Plant Analysis 37:525-539. https://doi.org/10.1080/00103620500449385
Caleja C, Barros L, Antonio A, Oliveira M, Ferreira I (2017). A comparative study between natural and synthetic antioxidants: Evaluation of their performance after incorporation into biscuits. Food Chemistry 216:342-346. https://doi.org/10.1016/j.foodchem.2016.08.075
Camejo D, Rodriguez P, Morales M, Dell’Amico J, Torrecillas A, Alarcon J (2005). High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. Journal of Plant Physiology 162:281-289. https://doi.org/10.1016/j.jplph.2004.07.014
Chao PY, Lin SY, Lin KH, Liu YF, Hsu JI, Yang CM, Lai JY (2014). Antioxidant activity in extracts of 27 indigenous Taiwanese vegetables. Nutrients 6:2115-2130. https://doi.org/10.3390/nu6052115
Chauhan NK, Singh S, Haider S, Lohani H, Kushwaha B (2013). Compositional variability in volatiles from different plant organs of Perilla frutescens L. cultivated in Uttarakhand (India). Journal of Pharmacy Research 6:361-363. https://doi.org/10.1016/j.jopr.2013.03.004
Chen Y, Wang E, Wei Z, Zheng Y, Yan R, Ma X (2019). Phytochemical analysis, cellular antioxidant, and α-glucosidase inhibitory activities of various herb plant organs. Industrial Crops and Products 141:111771. https://doi.org/10.1016/j.indcrop.2019.111771
Colica C, Di Renzo L, Aiello V, De Lorenzo A, Abenavoli L (2018). Rosmarinic acid as potential anti-inflammatory agent. Reviews on Recent Clinical Trials 13:240-242. https://doi.org/10.2174/157488711304180911095818
D’Ambrosio N, Arena C, De Santo AV (2006). Temperature response of photosynthesis, excitation energy dissipation and alternative electron sinks to carbon assimilation in Beta vulgaris L. Environmental and Experimental Botany 55:248-257. https://doi.org/10.1016/j.envexpbot.2004.11.006
Demmig-Adams B, Adams W, Barker DH, Logan BA, Bowlong DR, Verhoeven AS (1996). Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiologia Plantarum 98:253-264. https://doi.org/10.1034/j.1399-3054.1996.980206.x
Devitt DA, Morris RL, Fenstermaker LK (2005). Foliar damage, spectral reflectance, and tissue ion concentrations of trees sprinkle irrigated with waters of similar salinity but different chemical composition. HortScience 40:819-826. https://doi.org/10.21273/HORTSCI.40.3.819
Dhyani A, Chopra R, Garg M (2019). A review on nutritional value, functional properties, and pharmacological application of perilla (Perilla frutescens L.). Biomedical and Pharmacology Journal 12:649-660. https://doi.org/10.13128/ahs-23828
Diao M, Ma L, Wang J, Cui J, Fu A, Liu HY (2014). Selenium promotes the growth and photosynthesis of tomato seedlings under salt stress by enhancing chloroplast antioxidant defense system. Journal Plant Growth Regulation 33:671-682. https://doi.org/10.1007/s00344-014-9416-2
Ghane M, Mohammadi M, Pirdashti H (2019). Yield and physiological response of Perilla (Perilla frutescens) under different soil fertility treatments. Advances in Horticultural Science 33:205-214. https://doi.org/10.13128/ahs-23828
Ghanta S, Datta R, Bhattacharyya D, Sinha R, Kumar D, Hazra S, Mazumdar AB, Chattopadhyay S (2014). Multistep involvement of glutathione with salicylic acid and ethylene to combat environmental stress. Journal of Plant Physiology 171:940-950. https://doi.org/10.1016/j.jplph.2014.03.002
Ghimire BK, Yoo JH, Yu CY, Kim SH, Chung IM (2019). Profiling volatile and phenolic compound composition and characterization of the morphological and biological activities of Perilla frutescence Britton var. japonica accessions. Acta Physiologiae Plantarum 41:108. https://doi.org/10.1007/s11738-019-2890-1
Ghimire BK, Yoo H, Yu CY, Chung IM (2017). GC-MS analysis of volatile compounds of Perilla frutescens Britton var. Japonica accessions: Morphological and seasonal variability. Asian Pacific Journal of Tropical Medicine 10(7):643-651. https://doi.org/10.1016/j.apjtm.2017.07.004
Ha TJ, Lee JH, Lee MH, Lee BW, Kwon HS, Park CH, … Jang DS (2012). Isolation and identification of phenolic compounds from the seeds of Perilla frutescens (L.) and their inhibitory activities against a-glucosidase and aldose refuctase. Food Chemistry 135:1397-1403. https://doi.org/10.1016/j.foodchem.2012.05.104
Habibi G (2018). Effects of mild and severe drought stress on the biomass, phenolic compounds production and photochemical activity of Aloe vera (L.) Burm.f. Acta Agriculturae Slovenica 2018:463-476. https://doi.org/10.14720/aas.2018.111.2.19
Hikosaka S, Iwamoto N, Goto E, Ching HC (2017). Effects of supplemental lighting on growth and medicinal compounds of Japanese Honysuckle Lonicera japonica Thunb. Environmental Control in Biology 55: 71-76. https://doi.org/10.2525/ecb.55.71
Hong E, Park KH, Kim GH (2011). Phenolic‐enriched fractions from Perilla frutescens var. acuta: Determinating rosmarinic acid and antioxidant activity. Journal of Food Biochemistry 35:1637-1645. https://doi.org/10.1111/j.1745-4514.2010.00481.x
Huang C, Zhao S, Wang L, Anjum S, Chen M, Zou C (2013). Alteration in chlorophyll fluorescence, lipid peroxidation and antioxidant enzymes activities in hybrid ramie (Boehmeria nivea L.) under drought stress. Australian Journal of Crop Science 7:594-599. http://www.cropj.com/huang3003_7_5_2013_594_599.pdf
Janda M, Ruellan E (2015). Magical mystery tour: Salicylic acid signalling. Environmental and Experimental Botany 114:117-128. https://doi.org/10.1016/j.envexpbot.2014.07.003
Kagawa N, Iguchi H, Henzan M, Hanaoka M (2019). Drying the leaves of Perilla frutescens increases their content of anticancer nutraceuticals. Food Science and Nutrition 7:1494-1501 https://doi.org/10.1002/fsn3.993
Kheirizadeh-Arough Y, Seyed-Sharif R (2016). Biofertilizers and zinc effects on some physiological parameters of triticale under water-limitation condition. Journal of Plant Interactions 11:167-177. https://doi.org/10.1080/17429145.2016.1262914
Kiazolu JB, Intisar A, Zhang L, Wang Y, Zhang R, Wu Z (2016). Phytochemical screening and chemical variability in volatile oils of aerial parts of Morinda morindoides. Natural Product Research 30:2249-2252. https://doi.org/10.1080/14786419.2016.1154058
Kim SJ, Bok KJ, Lam VP, Park JS (2017). Response of nutrient solution and photosynthetic photon flux density for growth and accumulation of antioxidant in Agastache rugosa under hydroponic culture systems. Protected Horticulture and Plant Factory 26:249-257. https://doi.org/10.12791/KSBEC.2017.26.4.249
Kim YB, Kim JK, Uddin MR, Xu HH, Park WT, Tuan PA, … Park SU (2013). Metabolomics analysis and biosynthesis of rosmarinic acid in Agastache rugosa Kuntze treated with methyl jasmonate. PLoS One 8:e64199. https://doi.org/10.1371/journal.pone.0064199
Kozai T, Niu G, Takagaki M (2015). Plant factory: An indoor vertical farming system for efficient quality food production. Amsterdam: Academic Press.
Lee YH, Kim B, Kim S, Kim MS, Kim H, Hwang SR, Lee JH (2017). Characterization of metabolite profiles from the leaves of green perilla (Perilla frutescens) by ultra-high-performance liquid chromatography coupled with electrospray ionization quadrupole time-of-flight mass spectrometry and screening for their antioxidant properties. Journal of Food and Drug Analysis 25:776-788. https://doi.org/10.1016/j.jfda.2016.09.003
Levizou E, Drilias P, Psaras GK, Maneta Y (2005). Nondestructive assessment of leaf chemistry and physiology through spectral reflectance measurements may be misleading when changes in trichome density cooccur. New Phytologist 165:463-472. https://doi.org/10.1111/j.1469-8137.2004.01250.x
Lin T, Zhu X, Zhang F (2012). The interaction effect of cadmium and nitrogen on Populus yunnanensis. Journal of Agricultural Science 4:125-134.
Lin KH, Huang SB, Wu CW, Chang YS (2019). Effects of salicylic acid and calcium chloride on heat tolerance of Poinsettia. HortScience 54:499-504. https://doi.org/10.21273/HORTSCI13566-18
Liu J, Wan Y, Zhao Z, Chen H (2013). Determination of the content of rosmarinic acid by HPLC and analytical comparison of volatile constituents by GC-MS in different parts of Perilla frutescens (L.) Britt. Chemistry Central Journal 7:61. https://doi.org/10.1186/1752-153X-7-61
Lu N, Takagaki M, Yamori W, Kagawa N (2018). Flavonoid productivity optimized for green and red forms of Perilla frutescens via environmental control technologies in plant factory. Journal of Food Quality 2018:4270279. https://doi.org/10.1155/2018/4270279
Lu N, Bernardo EL, Tippayadarapanich C, Takagaki M, Kagawa N, Yamori W (2017). Growth and accumulation of secondary metabolites in perilla as affected by photosynthetic photon flux density and electrical conductivity of the nutrient solution. Frontiers in Plant Science 8:708. https://doi.org/10.3389/fpls.2017.00708
Marin A, Rubio JS, Martinez V, Gil MI (2009). Antioxidant compounds in green and red peppers as affected by irrigation frequency, salinity and nutrient solution composition. Journal of the Science of Food and Agriculture 89:1352-1359. https://doi.org/10.1002/jsfa.3594
Martinetti L, Ferrante A, Bassoli A, Borgonovo G, Tosca A, Spoleto P (2012). Characterization of some qualitative traits in different perilla cultivars. Acta Horticulturae 939:301-308. https://doi.org/10.17660/ActaHortic.2012.939.39
Naczk M, Shahidi F (2004). Extraction and analysis of phenolic in food. Journal of Chromatography A 1054:95-111.
Ogawa E, Hikosaka S, Goto E (2018). Effects of nutrient solution temperature on the concentration of major bioactive compounds in red perilla. Journal of Agricultural Meteorology 74:71-78. https://doi.org/10.2480/agrmet.D-17-00037
Osakabe N, Yasuda A, Natsume M, Sanbongi C, Kato Y, Osawa T, Yoshikawa T (2002). Rosmarinic acid, a major polyphenolic component of Perilla frutescens, reduces lipopolysaccharide (LPS)-induced liver injury in D-galactosamine (D-GalN)- sensitized mice. Free Radical Biology and Medicine 33:798-806. https://doi.org/10.1016/s0891-5849(02)00970-x
Park SY, Oh SB, Kim SM, Cho YY, Oh MM (2016). Evaluating the effects of a newly developed nutrient solution on growth, antioxidants, and chicoric acid contents in Crepidiastrum denticulatum. Horticulture, Environment, and Biotechnology 57:478-486. https://doi.org/10.1007%2Fs13580-016-1060-2
Pintha K, Tantipaiboonwong P, Yodkeeree S, Chaiwangyen W, Chumphukam O, Khantamat O, … Suttajit M (2018). Thai perilla (Perilla frutescens) leaf extract inhibits human breast cancer invasion and migration. Maejo International Journal of Science and Technology 12:112-123.
Saeb K, Gholamrezaee S (2012). Variation of essential oil composition of Melissa officinalis L. leaves during different stages of plant growth. Asian Pacific Journal of Tropical Biomedicine 2:547-549.
Sakamoto M, Suzuki T (2015). Effect of root-zone temperature on growth and quality of hydroponically grown red leaf lettuce (Lactuca sativa L. cv. Red Wave). American Journal of Plant Sciences 6:2350-2360. https://doi.org/10.4236/ajps.2015.614238
Selmar D, Kleinwächter M (2013). Stress enhances the synthesis of secondary plant products: the impact of the stress-related over-reduction on the accumulation of natural products. Plant and Cell Physiology 54:817-826. https://doi.org/10.1093/pcp/pct054
Skowyra M, Falguera V, Azman NA, Segovia F, Almajano MP (2014). The effect of Perilla frutescens extract on the oxidative stability of model food emulsions. Antioxidants3:38-54. https://doi.org/10.3390/antiox3010038
Shen H, B Zhao, J Xu, X Zheng, W Huang (2016). Effects of salicylic acid and calcium chloride on heat tolerance in Rhododendron ‘Fen Zhen Zhu’. Journal of the American Society for Horticultural Science 141:363-372. https://doi.org/10.21273/JASHS.141.4.363
Sivanandhan G, Arun M, Mayavan S, Rajesh M, Mariashibu TS, Manickavasagam M, … Ganapathi A (2012). Chitosan enhances withanolides production in adventitious root cultures of Withania somnifera (L.). Dunal. Industry Crops and Products 37:124-129. https://doi.org/10.1016/j.indcrop.2011.11.022
Swamy MK, Sinniah UR, Ghasemzadeh A (2018). Anticancer potential of rosmarinic acid and its improved production through biotechnological interventions and functional genomics. Applied Microbiology Biotechnology 102:7775-7793. https://doi.org/10.1007/s00253-018-9223-y
Taga MS, Miller EE, Pratt DE (1984). Chia seeds as a source of natural lipid antioxidants. Journal American Oil Chemistry Society 61:928-931. https://doi.org/10.1007/BF02542169
Umakanta S, Oba S (2018). Response of nutrients, minerals, antioxidant leaf pigments, vitamins, polyphenol, flavonoid and antioxidant activity in selected vegetable amaranth under four soil water content. Food Chemistry 252:72-83. https://doi.org/10.1016/j.foodchem.2018.01.097
Weng JH, Jhaung LH, Lin RJ, Chen HY (2010). Relationship between photochemical efficiency of photosystem II and the photochemical reflectance index of mango tree: Merging data from different illuminations, seasons, and leaf colors. Tree Physiology 30:469-478. https://doi.org/10.1093/treephys/tpq007
Whitehead D, Boelman NT, Turnbull MH, Griffin KL, Tissue DY, Barbour MM, … Peltzer DA (2005). Photosynthesis and reflectance indices for rainforest species in ecosystems undergoing progression and retrogression along a soil fertility chronosequence in New Zealand. Oecologia 144:233-244.
Wu CW, Lin KH, Lee MC, Peng YL, Chou TY, Chang YS (2015). Using chlorophyll fluorescence and vegetation indices to predict the timing of nitrogen demand in Pentas lanceolata. Korean Journal Horticulture Science Technology 33:845-853.
Yamori W (2016). Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress. Journal Plant Research 129:379-395. https://doi.org/10.1007/s10265-016-0816-1
Yoshiki Y, Kahhara T, Sakabe S, Yamasaki T (2001). Superoxide and DPPH radical-scavenging activities of soyasponin beta bg related to gallic acid. Bioscience Biotechnology Biochemistry 65:2162-2165. https://doi.org/10.1271/bbb.65.2162
Yoshimatsu K (2012). Innovative cultivation: Hydroponics of medicinal plants in the closed-type cultivation facilities. Journal of Traditional Medicines 29:30-34. https://doi.org/10.11339/jtm.29.30
Zhao Y, Kong H, Zhang X, Hu X, Wang M (2019). The effect of Perilla (Perilla frutescens) leaf extracts on the quality of surimi fish balls. Food Science and Nutrition 7:2083-2090. https://doi.org/10.1002/fsn3.1049
Zhou X, Yan L, Yin P, Shi L, Zhang L, Liu L, Ma C (2014). Structural characterisation and antioxidant activity evaluation of phenolic compounds from cold-pressed Perilla frutescens var. arguta seed flour. Food Chemistry 164:150-157. https://doi.org/10.1016/j.foodchem.2014.05.062
Zou J (2011). Proteomics of rice in response to heat stress and advances in genetic engineering for heat tolerance in rice. Plant Cell Report 30:2155-2165. https://doi.org/10.1007/s00299-011-1122-y
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