Skip to main navigation menu Skip to main content Skip to site footer
Plant Science Today (PST)

Research Articles

Early Access

Effect of different NaCl concentrations on secondary metabolites and antioxidant activity in three radish (Raphanus sativus L.) varieties

DOI
https://doi.org/10.14719/pst.3969
Submitted
24 May 2024
Published
22-11-2024
Versions

Abstract

Salinity, a critical environmental stressor, imposes constraints on field crops' anatomical structure, growth, and physiology. This study has uniquely evaluated the effect of 0 (control), 100, and 200 mM NaCl on phenolic acids (PAs), total anthocyanin content (TAC), chlorophyll, and antioxidant activity in three radish varieties and contributes novel insights to the scientific co community. The salt concentration significantly influenced shoot length (SL), root length (RL), and fresh weight (FW) in radish sprouts. The varying salt concentrations did not affect chlorophyll a, but chlorophyll b and total chlorophyll content (TCC) increased the red and super red varieties. The total phenolic content (TPC) and total flavonoid content (TFC) registered a slight increase in some varieties under 100 mM salt concentration, with the highest accumulation of these secondary metabolites found in the super red variety. Five individual PAs were identified using high-performance liquid chromatography (HPLC) analysis, with salt treatment significantly affecting ferulic acid and trans-cinnamic acid concentrations. The lowest level of anthocyanin was found in all green varieties. Salinity stress of 100 and 200 mM affected the TAC in the red and super red varieties compared to the control. Furthermore, among the three varieties treated with NaCl, the super red IC50 values displayed the highest 2,2,1-diphenyl-1-picrylhydrazyl (DPPH) and 2,2-Azino-bis-3-ethylbenzothiazoline-6-sulfonic Acid (ABTS) free radical scavenging activity compared to the other treatments. These results suggest that a 100 mM NaCl concentration can be used as an inducer to improve the accumulation of phytochemicals in the radish seedlings 12 days after sowing (DAS).

References

  1. Banihani SA. Radish (Raphanus sativus) and diabetes. Nutrients. 2017;9(9):1014. https://doi.org/https://doi.org/10.3390/nu9091014
  2. Popper PAM. Food over medicine: The conversation that could save your life. BenBella Books; Dallas; TX; USA 2014.
  3. Rasool S, Hameed A, Azooz MM, Muneeb-u-Rehman, Siddiqi TO, Ahmad P. Salt stress: Causes, types and responses of plants. In: Ahmad P, Azooz M, Prasad M, editors. Ecophysiology and Responses of Plants under Salt Stress; New York: Springer; 2013.p.01-24. https://doi.org/10.1007/978-1-4614-4747-4_1
  4. Kordrostami M, Rabiei B. Salinity stress tolerance in plants: Physiological, molecular and biotechnological approaches. In Hasanuzzaman M, Hakeem KR, Nahar K, Alharby HF, editors. Plant Abiotic Stress Tolerance: Agronomic, Molecular and Biotechnological Approaches; Berlin/Heidelberg, Springer; 2019.p.101-127. https://doi.org/https://doi.org/10.1007/978-3-030-06118-0_4
  5. Shahid SA, Zaman M, Heng L. Soil salinity: Historical perspectives and a world overview of the problem. In Zaman M, Shahid SA, Heng L, editors. Guideline for Salinity Assessment, Mitigation and Adaptation Using Nuclear and Related Techniques; Cham, Springer; 2018.p.43-53. https://doi.org/https://doi.org/10.1007/978-3-319-96190-3
  6. Machado RMA, Serralheiro RP. Soil salinity: Effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulturae. 2017;3(2):30. https://doi.org/https://doi.org/10.3390/horticulturae3020030
  7. Akula R, Ravishankar GA. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal. Behav. 2011;6(11):1720-31. https://doi.org/https://doi.org/10.4161/psb.6.11.17613
  8. Shen Q, Fu L, Dai F, Jiang L-x, Zhang G-p, Wu D. Multi-omics analysis reveals molecular mechanisms of shoot adaption to salt stress in Tibetan wild barley. BMC Genomics. 2016;17(1):889. https://doi.org/https://doi.org/10.1186/s12864-016-3242-9
  9. Abdullahil Baque M, Lee E-J, Paek K-Y. Medium salt strength induced changes in growth, physiology and secondary metabolite content in adventitious roots of Morinda citrifolia: the role of antioxidant enzymes and phenylalanine ammonia lyase. Plant Cell Rep. 2010;29(7):685-94. https://doi.org/https://doi.org/10.1007/s00299-010-0854-4
  10. Wang Y, Stevanato P, Yu L, Zhao H-j, Sun X, Sun F, et al. The physiological and metabolic changes in sugar beet seedlings under different levels of salt stress. J. Plant Res. 2017;130(6):1079-93. https://doi.org/https://doi.org/10.1007/s10265-017-0964-y
  11. Munns R, Tester MA. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 2008;59(1):651-81. https://doi.org/https://doi.org/10.1146/annurev.arplant.59.032607.092911
  12. Vicente Ó, Boscaiu M, Naranjo MA, Estrelles E, Bellés JM, Soriano P. Responses to salt stress in the halophyte Plantago crassifolia (Plantaginaceae). J. Arid Environ. 2004;58(4):463-81. https://doi.org/https://doi.org/10.1016/j.jaridenv.2003.12.003
  13. Elshafie HS, Camele I, Mohamed AA. A comprehensive review on the biological, agricultural and pharmaceutical properties of secondary metabolites based-plant origin. Int. J. Mol. Sci. 2023;24(4):3266. https://doi.org/https://doi.org/10.3390/ijms24043266
  14. Marchev AS, Yordanova ZP, Georgiev MI. Green (cell) factories for advanced production of plant secondary metabolites. Crit. Rev. Biotechnol. 2020;40(4):443-58. https://doi.org/https://doi.org/10.1080/07388551.2020.1731414
  15. Wani AK, Akhtar N, Sharma AK, El-Zahaby SA. Fighting carcinogenesis with plant metabolites by weakening proliferative signaling and disabling replicative immortality networks of rapidly dividing and invading cancerous cells. Curr. Drug Deliv. 2022;20(4):371-86. https://doi.org/https://doi.org/10.2174/1567201819666220414085606
  16. Yuan G, Wang X, Guo R, Wang Q-M. Effect of salt stress on phenolic compounds, glucosinolates, myrosinase and antioxidant activity in radish sprouts. Food Chem. 2010;121(4):1014-19. https://doi.org/https://doi.org/10.1016/j.foodchem.2010.01.040
  17. Ritchie RJ. Universal chlorophyll equations for estimating chlorophylls a, b, c and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol or ethanol solvents. Photosynthetica. 2008;46(1):115-26. https://doi.org/https://doi.org/10.1007/s11099-008-0019-7
  18. Porra RJ, Scheer H. Towards a more accurate future for chlorophyll a and b determinations: the inaccuracies of Daniel Arnon’s assay. Photosynth. Res. 2018;140(1):215-19. https://doi.org/https://doi.org/10.1007/s11120-018-0579-8
  19. Lee SY, Kwon H-R, Kim JK, Park CH, Sathasivam R, Park S-U. Comparative analysis of glucosinolate and phenolic compounds in green and red kimchi cabbage (Brassica rapa L. ssp. pekinensis) hairy roots after exposure to light and dark conditions. Horticulturae. 2023;9(4):466. https://doi.org/https://doi.org/10.3390/horticulturae9040466
  20. Febriany S, Wulandari P, Suparto IH, Ridwan T, Rahayu S, Siswoyo DM. Total phenolics, flavonoids and anthocyanin contents of six Vireya rhododendron from Indonesia and evaluation of their antioxidant activities. J. Appl. Pharm. Sci. 2018;88(9):49-54. https://doi.org/http://dx.doi.org/10.7324/JAPS.2018.8908
  21. Dhanani T, Shah S, Gajbhiye N, Kumar S. Effect of extraction methods on yield, phytochemical constituents and antioxidant activity of Withania somnifera. Arab. J. Chem. 2017;10(1):1193-99. https://doi.org/https://doi.org/10.1016/j.arabjc.2013.02.015
  22. Saeed N, Khan MR, Shabbir M. Antioxidant activity, total phenolic and total flavonoid contents of whole plant extracts Torilis leptophylla L. BMC Complement. Altern. Med. 2012;12:221. https://doi.org/https://doi.org/10.1186/1472-6882-12-221
  23. de Menezes BB, Frescura LM, Duarte RB, Villetti MA, da Rosa MB. A critical examination of the DPPH method: Mistakes and inconsistencies in stoichiometry and IC50 determination by UV-Vis spectroscopy. Anal. Chim. Acta. 2021;1157:338398. https://doi.org/https://doi.org/10.1016/j.aca.2021.338398
  24. Arnao MB, Cano A, Acosta M. The hydrophilic and lipophilic contribution to total antioxidant activity. Food Chem. 2001;73(2):239-44. https://doi.org/https://doi.org/10.1016/S0308-8146(00)00324-1
  25. Ferreira ICFR, Baptista P, Vilas-Boas M, Barros L. Free-radical scavenging capacity and reducing power of wild edible mushrooms from northeast Portugal: individual cap and stipe activity. Food Chem. 2007;100(4):1511-16. https://doi.org/https://doi.org/10.1016/j.foodchem.2005.11.043
  26. Gülçin I. Fe(3+)-Fe(2+) transformation method: an important antioxidant assay. Methods Mol. Biol. 2015;1208:233-46. https://doi.org/https://doi.org/10.1007/978-1-4939-1441-8_17
  27. Adetunji AE, Sershen, Varghese B, Pa mMenter NW. Effects of inorganic salt solutions on vigour, viability, oxidative metabolism and germination enzymes in aged cabbage and lettuce seeds. Plants. 2020;9(9):1164. https://doi.org/https://doi.org/10.3390/plants9091164
  28. Manaa A, Goussi R, Derbali W, Cantamessa S, Abdelly C, Barbato R. Salinity tolerance of quinoa (Chenopodium quinoa Willd) as assessed by chloroplast ultrastructure and photosynthetic performance. Environ. Exp. Bot. 2019;162(1):103-14. https://doi.org/https://doi.org/10.1016/j.envexpbot.2019.02.012
  29. Fariduddin Q, Varshney P, Yusuf M, Ali A, Ahmad A. Dissecting the role of glycine betaine in plants under abiotic stress. Plant Stress. 2013;7(1):08-18.
  30. Lim JH, Park K-J, Kim B-K, Jeong J-W, Kim H-J. Effect of salinity stress on phenolic compounds and carotenoids in buckwheat (Fagopyrum esculentum M.) sprout. Food Chem. 2012;135(3):1065-70. https://doi.org/https://doi.org/10.1016/j.foodchem.2012.05.068
  31. Pungin A, Lartseva L, Loskutnikova V, Shakhov V, Popova E, Skrypnik LN, et al. Effect of salinity stress on phenolic compounds and antioxidant activity in halophytes Spergularia marina (L.) Griseb. and Glaux maritima L. cultured in vitro. Plants. 2023;12(9):1905. https://doi.org/https://doi.org/10.3390/plants12091905
  32. Kaouther Z, Mariem BF, Fardaous M, Chérif H. Impact of salt stress (NaCl) on growth, chlorophyll content and fluorescence of Tunisian cultivars of chili pepper (Capsicum frutescens L.). J. Stress Physiol. Biochem. 2012;8(4):236-52.
  33. Zahra N, Al Hinai MS, Hafeez MB, Rehman A, Wahid A, Siddique KHM, et al. Regulation of photosynthesis under salt stress and associated tolerance mechanisms. Plant Physiol. Biochem. 2022;178:55-69. https://doi.org/https://doi.org/10.1016/j.plaphy.2022.03.003
  34. Li J, Ma J, Guo H, Zong J, Chen J, Wang Y, et al. Growth and physiological responses of two phenotypically distinct accessions of centipedegrass (Eremochloa ophiuroides (Munro) Hack.) to salt stress. Plant Physiol. Biochem. 2018;126:01-10. https://doi.org/https://doi.org/10.1016/j.plaphy.2018.02.018
  35. Tanaka H, Yamada S, Masunaga T, Yamamoto S, Tsuji W, Murillo-Amador B. Comparison of nutrient uptake and antioxidative response among four Labiatae herb species under salt stress condition. Soil Sci. Plant Nutr. 2018;64(5):589-97. https://doi.org/https://doi.org/10.1080/00380768.2018.1492334
  36. Taïbi K, Taïbi F, Abderrahim LA, Ennajah A, Belkhodja M, Mulet JM. Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. S. Afr. J. Bot. 2016;105:306-12. https://doi.org/https://doi.org/10.1016/j.sajb.2016.03.011
  37. Qados AMSA. Effect of salt stress on plant growth and metabolism of bean plant Vicia faba (L.). J. Saudi Soc. Agric. Sci. 2011;10:07-15. https://doi.org/https://doi.org/10.1016/j.jssas.2010.06.002
  38. Castillo JM, Mancilla-Leytón JM, Martins-Noguerol R, Moreira X, Moreno-Pérez AJ, Muñoz-Vallés S, et al. Interactive effects between salinity and nutrient deficiency on biomass production and bio-active compounds accumulation in the halophyte Crithmum maritimum. Sci. Hortic. 2022;301:111136. https://doi.org/https://doi.org/10.1016/j.scienta.2022.111136
  39. Ghanem AE-MFM, Mohamed E, Kasem A MMA, El-Ghamery AA. Differential salt tolerance strategies in three halophytes from the same ecological habitat: Augmentation of antioxidant enzymes and compounds. Plants. 2021;10(6):1100. https://doi.org/https://doi.org/10.3390/plants10061100
  40. Kim H-J, Fonseca JM, Choi J-H, Kubota C, Kwon DY. Salt in irrigation water affects the nutritional and visual properties of romaine lettuce (Lactuca sativa L.). J. Agric. Food Chem. 2008;56(10):3772-76. https://doi.org/https://doi.org/10.1021/jf0733719
  41. López-Berenguer C, Martínez-Ballesta MdC, Moreno DA, Carvajal M, García-Viguera C. Growing hardier crops for better health: Salinity tolerance and the nutritional value of broccoli. J. Agric. Food Chem. 2009;57(2):572-78. https://doi.org/https://doi.org/10.1021/jf802994p
  42. Navarro JM, Flores P, Garrido C, Martínez V. Changes in the contents of antioxidant compounds in pepper fruits at different ripening stages, as affected by salinity. Food Chem. 2006;96(1):66-73. https://doi.org/https://doi.org/10.1016/j.foodchem.2005.01.057
  43. Hichem H, Mounir D, Naceur EA. Differential responses of two maize (Zea mays L.) varieties to salt stress: Changes on polyphenols composition of foliage and oxidative damages. Ind. Crops Prod. 2009;30(1):144-51. https://doi.org/https://doi.org/10.1016/j.indcrop.2009.03.003
  44. Valifard M, Mohsenzadeh S, Kholdebarin B, Rowshan V. Effects of salt stress on volatile compounds, total phenolic content and antioxidant activities of Salvia mirzayanii. S. Afr. J. Bot. 2014;93:92-97. https://doi.org/https://doi.org/10.1016/j.sajb.2014.04.002
  45. Bistgani ZE, Hashemi M, Dacosta MA, Craker LE, Maggi F, Morshedloo MR. Effect of salinity stress on the physiological characteristics, phenolic compounds and antioxidant activity of Thymus vulgaris L. and Thymus daenensis Celak. Ind. Crops Prod. 2019;135(1):311-20. https://doi.org/https://doi.org/10.1016/j.indcrop.2019.04.055
  46. Lini? I, Šamec D, Grúz J, Vuj?i? Bok V, Strnad M, Salopek-Sondi B. Involvement of phenolic acids in short-term adaptation to salinity stress is species-specific among Brassicaceae. Plants. 2019;8(6):155. https://doi.org/https://doi.org/10.3390/plants8060155
  47. Sarker U, Oba S. Augmentation of leaf color parameters, pigments, vitamins, phenolic acids, flavonoids and antioxidant activity in selected Amaranthus tricolor under salinity stress. Sci. Rep. 2018;8:12349. https://doi.org/https://doi.org/10.1038/s41598-018-30897-6
  48. Docimo T, De Stefano R, Cappetta E, Piccinelli AL, Celano R, De Palma M, et al. Physiological, biochemical and metabolic responses to short and prolonged saline stress in two cultivated cardoon genotypes. Plants. 2020;9(5):554. https://doi.org/https://doi.org/10.3390/plants9050554
  49. Kiani R, Arzani A, Mirmohammady Maibody SAM. Polyphenols, flavonoids and antioxidant activity involved in salt tolerance in wheat, Aegilops cylindrica and their amphidiploids. Front. Plant Sci. 2021;12:646221. https://doi.org/https://doi.org/10.3389/fpls.2021.646221
  50. Farooq M, Ahmad R, Shahzad MI, Sajjad Y, Hassan A, Shah MM, et al. Differential variations in total flavonoid content and antioxidant enzymes activities in pea under different salt and drought stresses. Sci. Hortic. 2021;287:110258. https://doi.org/https://doi.org/10.1016/j.scienta.2021.110258
  51. Kim J, Lee WJ, Vu TT, Jeong CY, Hong S-W, Lee H. High accumulation of anthocyanins via the ectopic expression of AtDFR confers significant salt stress tolerance in Brassica napus L. Plant Cell Rep. 2017;36(8):1215-24. https://doi.org/https://doi.org/10.1007/s00299-017-2147-7
  52. Saad KR, Kumar G, Mudliar SN, Giridhar P, Shetty NP. Salt stress-induced anthocyanin biosynthesis genes and MATE transporter involved in anthocyanin accumulation in Daucus carota cell culture. ACS Omega. 2021;6(38):24502-14. https://doi.org/https://doi.org/10.1021/acsomega.1c02941
  53. Thabet SG, Alomari DZ, Alqudah AM. Exploring natural diversity reveals alleles to enhance antioxidant system in barley under salt stress. Plant Physiol. Biochem. 2021;166:789-98. https://doi.org/https://doi.org/10.1016/j.plaphy.2021.06.030
  54. Liang W, Ma X, Wan P, Liu L. Plant salt-tolerance mechanism: A review. Biochem. Biophys. Res. Commun. 2018;495(1):286-91. https://doi.org/https://doi.org/10.1016/j.bbrc.2017.11.043
  55. Jahantigh O, Najafi F, Badi HN, Khavari-Nejad RA, Sanjarian F. Changes in antioxidant enzymes activities and proline, total phenol and anthocyanin contents in Hyssopus officinalis L. plants under salt stress. Acta Biol. Hung. 2016;67(2):195-204. https://doi.org/https://doi.org/10.1556/018.67.2016.2.7
  56. Mbarki S, Sytar O, Živ?ák M, Abdelly C, Cerdà A, Bresti? M. Anthocyanins of coloured wheat genotypes in specific response to salt stress. Molecules. 2018;23(7):1518. https://doi.org/https://doi.org/10.3390/molecules23071518
  57. Ery?lmaz F. The relationships between salt stress and anthocyanin content in higher plants. Biotechnol. Biotechnol. Equip. 2006;20(1):47-52. https://doi.org/https://doi.org/10.1080/13102818.2006.10817303
  58. Chunthabur S, Sakuanrung S, Wongwarat T, Sanitchon J, Pattanagul W, Theerakulp P. Changes in anthocyanin content and expression of anthocyanin synthesis genes in seedlings of black glutinous rice in response to salt stress. Asian J. Plant Sci. 2016;15(4):56-65. https://doi.org/https://doi.org/10.3923/ajps.2016.56.65
  59. Kim SY, Lim J-H, Park MR, Kim YJ, Park T-i, Seo YW, et al. Enhanced antioxidant enzymes are associated with reduced hydrogen peroxide in barley roots under saline stress. J Biochem. Mol. Biol. 2005;38(2):218-24. https://doi.org/https://doi.org/10.5483/bmbrep.2005.38.2.218
  60. Elkahoui S, Hernández JA, Abdelly C, Ghrir R, Limam F. Effects of salt on lipid peroxidation and antioxidant enzyme activities of Catharanthus roseus suspension cells. Plant Sci. 2005;168(3):607-13. https://doi.org/https://doi.org/10.1016/j.plantsci.2004.09.006
  61. Rahnama H, Ebrahimzadeh H. The effect of NaCl on antioxidant enzyme activities in potato seedlings. Biol. Plant. 2005;49:93-97. https://doi.org/https://doi.org/10.1007/s10535-005-3097-4
  62. Jebara SH, Jebara M, Limam F, Aouani ME. Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. J Plant Physiol. 2005;162(8):929-36. https://doi.org/https://doi.org/10.1016/j.jplph.2004.10.005
  63. Ciriello M, Formisano L, Kyriacou MC, Carillo P, Scognamiglio L, De Pascale S, et al. Morpho-physiological and biochemical responses of hydroponically grown basil cultivars to salt stress. Antioxidants. 2022;11(11):2207. https://doi.org/https://doi.org/10.3390/antiox11112207

Downloads

Download data is not yet available.