Abstract
The genus Allium includes hundreds of plant species and is regarded as one of the most cultivated vegetables. It is an important source of novel therapeutic compounds known for their beneficial effects on human health; however, there could be differences in content, composition, type, and bioactivity of the phytochemicals found among the Allium plants. The main purpose of this study was to acquire insights on the variation in antioxidant profiles and phenolic content between Allium accessions in different species, as well as between similar species of several varieties. We collected 112 accessions from more than 20 countries, and grew them under similar agronomic conditions. The antioxidant potential was evaluated by using 2,2′-azino-bis-3-ethylbenzthiazoline-6-sulphonic acid (ABTS), 1,1-diphenyl-1-picrylhydrazyl (DPPH), ferric reducing antioxidant power (FRAP), and reducing power (RP) assays. The total phenolic content (TPC) was studied using the Folin–Ciocalteu method. TPC varied from 3.43 (accession 199897) to 22.19 (accession 273483) µg gallic acid equivalent/mg dry weight (DW) of the aerial organs of Allium. The antioxidant activity of Allium samples ranged from 4.37 (accession 806595) to 57.46 (accession number 711971) µg Trolox equivalent/mg DW; 0.35 (accession 117246) to 9.53 (accession 711971) µg ascorbic acid equivalents/mg DW; 2.92 (accession 199890) to 21.20 (accession 803493) µgAAE/mg DW; and 0.80 (accession 117260) to 31.13 (accession 803527) µgAAE/mg DW using ABTS, DPPH, FRAP, and RP assays, respectively. Accessions 273483 (A. cepa), 283346 (A. cepa ‘cepa’), and 803527 (unknown species) had the highest TPC, FRAP, and RP values among those tested, while the highest ABTS and DPPH radical scavenging activities were recorded in accession 711971 (A. ramosum). Pearson’s coefficient of correlations indicated that variables (TPC, ABTS, DPPH, FRAP, and RP values) correlated significantly each other, with r-values between 0.585 and 0.894. Principal component analysis plots and hierarchical cluster analysis indicated significant variability in antioxidant activity and phenolic content among all the accessions studied, as well as within similar species. Based on our results from principal component and hierarchical cluster analysis, accession 283346 (A. cepa ‘cepa’), K139348 (A. fistulosum), and 711971 (A. ramosum) are potential sources of phenolics and natural antioxidants. The variability in total phenolic and antioxidant activity among the Allium accessions can be used by breeders, food technologists, nutritionist, and researchers for assessing breeding lines for genetic selection and for monitoring levels of these factors during food storage and processing.
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References
Andarwulan N, Kurniasih D, Apriady RA, Rahmat H, Roto AV, Bolling BW (2012) Polyphenols, carotenoids, and ascorbic acid in underutilized medicinal vegetables. J Funct Foods 4:339–347
Awika JM, Rooney LW, Wu X, Prior RL, Cisneros-Zevallos L (2003) Screening methods to measure antioxidant activity of sorghum (Sorghum bicolor) and sorghum products. J Agric Food Chem 51:6657–6662
Beato VM, Orgaz F, Mansilla F, Montano A (2011) Changes in phenolic compounds in garlic (Allium sativum L.) Owing to the cultivar and location of growth. Plant Foods Hum Nutr 66:218–223
Benkeblia N (2005) Free-radical scavenging capacity and antioxidant properties of some selected Onions (Allium cepa L.) and garlic (Allium sativum L.) extracts. Braz Arch Biol Technol 48:753–759
Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76
Bernaert N, De Paepe D, Bouten C, De Clercq H, Stewart D, Van Bockstaele E, De Loose M, Van Droogenbroeck B (2012) Antioxidant capacity, total phenolic and ascorbate content as a function of the genetic diversity of leek (Allium ampeloprasum var. porrum). Food Chem 134:669–677
Block E (1992) The organosulfur chemistry of the genus Allium - implications for the organic chemistry of sulfur. Angew Chem Int Ed Engl 31:1135–1178
Block E, Naganathan S, Putman D, Zhao SH (1992) Allium chemistry—HPLC analysis of thiosulfinates from onion, garlic, wild garlic (ramsoms), leek, scallion, shallot, elephant (great-headed) garlic, chive, and Chinese chive—uniquely high allyl to methyl ratios in some garlic samples. J Agric Food Chem 40:2418–2430
Booth VH, Bradford MP (1963) Tocopherol contents of vegetables and fruits. Br J Nutr 17:575–581
Bozin B, Mimica-Dukic N, Samojlik I, Goran A, Igic R (2008) Phenolics as antioxidants in garlic (Allium sativum L., Alliaceae). Food Chem 111:925–929
Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT Food Sci Technol 28:25–30
Celep F, Koyuncu M, Fritsch RM, Kahraman A, Doğan M (2012) Taxonomic importance of seed morphology in Allium (Amaryllidaceae). Syst Bot 37:893–912
Ching LS, Mohamed S (2001) Alpha-tocopherol content in 62 edible tropical plants. J Agric Food Chem 49:3101–3105
Deng GF, Lin X, Xu XR, Gao LL, Xie JF, Li HB (2013) Antioxidant capacities and total phenolic contents of 56 vegetables. J Funct Foods 5:260–266
Dorsch W (1997) Allium cepa L (onion) part 2: chemistry, analysis and pharmacology. Phytomedicine 3:391–397
Fossen T, Andersen OM, Ovstedal DO, Pedersen AT, Raknes A (1996) Characteristic anthocyanin pattern from onions and other Allium spp. J Food Sci 61:703–706
Ghorbani A (2013) Best herbs for managing diabetes: a review of clinical studies. Braz J Pharm Sci 49:413–422
Gökçe AF, Kaya C, Serçe S, Özgen M (2010) Effect of scale color on the antioxidant capacity of onions. Sci Hortic (Amsterdam) 123:431–435
Goldman IL, Schwartz BS, Kopelberg M (1995) Variability in blood platelet inhibitory activity of Allium (Alliaceae) species accessions. Am J Bot 82:827–832
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1). http://palaeo-electronica.org/2001_1/past/issue1_01.htm
Hiyasat B, Sabha D, Grötzinger K, Kempfert J, Rauwald JW, Mohr FW, Dhein S (2009) Antiplatelet activity of Allium ursinum and Allium sativum. Pharmacology 83:197–204
Hsing AW, Chokkalingam AP, Gao YT et al (2002) Allium vegetables and risk of prostate cancer: a population-based study. J Natl Cancer Inst 94:1648–1651
Hwang IG, Woo KS, Kim DJ, Hong JT, Hwang BY, Lee YR, Jeong HS (2007) Isolation and identification of an antioxidant substance from heated garlic (Allium sativum L.). Food Sci Biotechnol 16:963–966
Karadag A, Ozcelik B, Saner S (2009) Review of methods to determine antioxidant capacities. Food Anal Methods 2:41–60
Kaur C, Joshi S, Kapoor HC (2009) Antioxidants in onion (Allium cepa L) cultivars grown in India. J Food Biochem 33:184–200
Kim JS, Ra JH, Hyun HN (2015) Comparison of biochemical composition and antimicrobial activity of southern-type garlic grown in the eastern and western regions of Jeju. Hortic Environ Biotechnol 33:763–771
Kogje KK, Jagdale VK, Dudhe SS, Phanikumar G, Badere RS (2010) Antioxidant property and phenolic compounds of few important plants from trans-Himalayan regions of North India. J Herb Med Toxicol 4:145–151
Kucekova Z, Mlcek J, Humpolicek P, Rop O, Valasek P, Saha P (2011) Phenolic compounds from Allium schoenoprasum, Tragopogon pratensis and Rumex acetosa and their antiproliferative effects. Molecules 16:9207–9217
Lachman J, Pronek D, Hejtmankova A (2003) Total polyphenol and main flavonoid antioxidants in different onion (Allium cepa L.) varieties. Hortic Sci 30:142–147
Lau BHS, Aetumbi MA (1983) Allium Sativum (Garlic) and atherosclerosis: a review. Nutr Res 3:119–128
Lawson LD (1998) Garlic: a review of its medicinal effects and indicated active compounds. In: Lawson LD, Bauer R (eds) Phytomedicines of Europe: chemistry and biological activity. ACS symposium series (No. 691). American Chemical Society, Washington, DC, pp 176–209
Lawson LD, Wood SG, Hughes BG (1991) HPLC analysis of allicin and other thiosulfinates in garlic clove homogenates. Planta Med 57:263–270
Lee J, Koo N, Min DB (2004) Reactive oxygen species, aging, and antioxidative nutraceuticals. Compr Rev Food Sci Food Saf 3:21–33
Lee J, Ha I, Kim H, Choi S, Lee S, Kang J, Boyhan GE (2016) Regional differences in onion bulb quality and nutrient content, and the correlation between bulb characteristics and storage loss. Korean J Hortic Sci Technol 34:807–817
Lemanska K, Szymusiak H, Tyrakowska B, Zielinski R, Soffers AEMF, Rietjens IMCM (2001) The influence of pH on antioxidant properties and the mechanism of antioxidant action of hydroxyflavones. Free Radic Biol Med 31:869–881
Li QQ, Zhou SD, He XJ, Yu Y, Zhang YC, Wei XQ (2010) Phylogeny and biogeography of Allium (Amaryllidaceae: allieae) based on nuclear ribosomal internal transcribed spacer and chloroplast rps16 sequences, focusing on the inclusion of species endemic to China. Ann Bot 106:709–733
Lu X, Ross CF, Powers JR, Aston DE, Rasco BA (2011a) Determination of total phenolic content and antioxidant activity of garlic (Allium sativum) and elephant garlic (Allium ampeloprasum) by attenuated total reflectance-fourier transformed infrared spectroscopy. J Agric Food Chem 59:5215–5221
Lu X, Wang J, Al-Qadiri HM, Ross CF, Powers JR, Tang J, Rasco BA (2011b) Determination of total phenolic content and antioxidant capacity of onion (Allium cepa) and shallot (Allium oschaninii) using infrared spectroscopy. Food Chem 129:637–644
Najjaa H, Zerria K, Fattouch S, Ammar E, Neffati M (2011) Antioxidant and antimicrobial activities of Allium roseum L. “Lazoul”, a wild edible endemic species in North Africa. Int J Food Prop 14:371–380
Nencini C, Cavallo F, Capasso A, Franchi GG, Giorgi G, Lucia M (2007) Evaluation of antioxidative properties of Allium species growing wild in Italy Cristina. Phyther Res 21:874–878
Nencini C, Menchiari A, Franchi GG, Micheli L (2011) In vitro antioxidant activity of aged extracts of some Italian Allium species. Plant Foods Hum Nutr 66:11–16
Nuutila AM, Puupponen-Pimia R, Aarni M, Oksman-Caldentey KM (2003) Comparison of antioxidant activities of onion and garlic extracts by inhibition of lipid peroxidation and radical scavenging activity. Food Chem 81:485–493
Ou B, Huang D, Hampsch-Woodill M, Flanagan JA, Deemer EK (2002) Analysis of antioxidant activities of common vegetables employing oxygen radical absorbance capacity (ORAC) and ferric reducing antioxidant power (FRAP) assays: a comparative study. J Agric Food Chem 50:3122–3128
Oyama SA, Amamoto YY (2007) Antioxidant activity and flavonoid content of Welsh onion (Allium fistulosum) and the effect of thermal treatment. Food Sci Technol Res 13:67–72
Park SY, Chin KB (2010) Evaluation of pre-heating and extraction solvents in antioxidant and antimicrobial activities of garlic, and their application in fresh pork patties. Int J Food Sci Technol 45:365–373
Piao XM, Jang EK, Chung JW, Lee GA, Lee HS, Sung JS, Jeon YA, Lee JR, Kim YG, Lee SY (2013) Variation in antioxidant activity and polyphenol content in tomato stems and leaves. Plant Breed Biotechnol 1:366–373
Powolny AA, Singh SV (2008) Multitargeted prevention and therapy of cancer by diallyl trisulfide and related Allium vegetable-derived organosulfur compounds. Cancer Lett 269:305–314
Prakash D, Singh BN, Upadhyay G (2007) Antioxidant and free radical scavenging activities of phenols from onion (Allium cepa). Food Chem 102:1389–1393
Prior RL, Wu X, Schaich K (2005) Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 53:4290–4302
Qu Z, Mossine VV, Cui J, Sun GY, Gu Z (2016) Protective effects of AGE and its components on neuroinflammation and neurodegeneration. NeuroMol Med 18:474–482
Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237
Rodríguez Galdón B, Rodríguez Rodríguez EM, Díaz Romero C (2008) Flavonoids in onion cultivars (Allium cepa L.). J Food Sci 73:C599–C605
Santas J, Almajano MP, Carbó R (2010) Antimicrobial and antioxidant activity of crude onion (Allium cepa, L.) extracts. Int J Food Sci Technol 45:403–409
Sharma K, Assefa AD, Kim S, Ko EY, Lee ET, Park SW (2014) Evaluation of total phenolics, flavonoids and antioxidant activity of 18 Korean onion cultivars: a comparative study. J Sci Food Agric 94:1521–1529
Siddiq M, Roidoung S, Sogi DS, Dolan KD (2013) Total phenolics, antioxidant properties and quality of fresh-cut onions (Allium cepa L.) treated with mild-heat. Food Chem 136:803–806
Singh BN, Singh BR, Singh RL, Prakash D, Singh DP, Sarma BK, Upadhyay G, Singh HB (2009) Polyphenolics from various extracts/fractions of red onion (Allium cepa) peel with potent antioxidant and antimutagenic activities. Food Chem Toxicol 47:1161–1167
Stajner D, Milic N, Canadanovic-Brunet J, Kapor A, Popovic B (2006) Exploring Allium species as a source of potential medicinal agents. Phyther Res 20:581–584
Štajner D, Popović BM, Ćalić-Dragosavac D, Malenčić Đ, Zdravković-Korać S (2011) Comparative study on Allium schoenoprasum cultivated plant and Allium schoenoprasum tissue culture organs antioxidant status. Phyther Res 25:1618–1622
Tepe B, Sokmen M, Akpulat HA, Sokmen A (2005) In vitro antioxidant activities of the methanol extracts of five Allium species from Turkey. Food Chem 92:89–92
Vu QH, Hang TTM, Yaguchi S, Ono Y, Pham TMP, Yamauchi N, Shigyo M (2013) Assessment of biochemical and antioxidant diversities in a shallot germplasm collection from Vietnam and its surrounding countries. Genet Resour Crop Evol 60:1297–1312
Waterhouse AL (2002) Determination of total phenolics. In: Wrolstad RE (ed) Current protocols in food analytical chemistry. Wiley, New York, pp I1.1.1–I1.1.8
Xiao H, Parkin KL (2002) Antioxidant functions of selected Allium thiosulfinates and S-alk(en)yl-l-cysteine sulfoxides. J Agric Food Chem 50:2488–2493
Yen GC, Chen HY (1995) Antioxidant activity of various tea extracts in relation to their antimutagenicity. J Agric Food Chem 43:27–32
Yin MC, Cheng WS (1998) Antioxidant activity of several Allium members. J Agric Food Chem 46:4097–4101
Zouari S, Najjaa H, Neffati M, Ammar E (2012) A new essential oil chemotype of Allium roseum analyzed by an apolar column. Int J Food Prop 15:385–397
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This study was conducted with the support from the Research Program for Agricultural Science & Technology Development (Project No.00937304), National Institute of Agricultural Sciences, Rural Development Administration, Republic of Korea.
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Assefa, A.D., Jeong, YJ., Kim, DJ. et al. Assessing phenolic content and antioxidant potential diversity in Allium plants using multivariate data analysis. Hortic. Environ. Biotechnol. 59, 759–773 (2018). https://doi.org/10.1007/s13580-018-0081-4
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DOI: https://doi.org/10.1007/s13580-018-0081-4