Comparative study of polyphenolic content and antioxidant capacity in fruits of Arbutus unedo, A. andrachne and their natural hybrid A.× andrachnoides

  • Konstantinos F. BERTSOUKLIS Agricultural University of Athens, School of Plant Sciences, Department of Crop Science, Laboratory of Floriculture and Landscape Architecture, Iera Odos 75, 11855 Athens (GR)
  • Ioannis DASKALAKIS Agricultural University of Athens, School of Plant Sciences, Department of Crop Science, Laboratory of Viticulture, Iera Odos 75, 11855 Athens (GR)
  • Katerina BINIARI Agricultural University of Athens, School of Plant Sciences, Department of Crop Science, Laboratory of Viticulture, Iera Odos 75, 11855 Athens (GR)
  • Maria PAPAFOTIOU Agricultural University of Athens, School of Plant Sciences, Department of Crop Science, Laboratory of Floriculture and Landscape Architecture, Iera Odos 75, 11855 Athens (GR)
Keywords: anthocyanins; eastern Mediterranean Arbutus; flavonoids; minor fruits; phenolics

Abstract

Fruits of the three Arbutus species native in the Eastern Mediterranean region, i.e. Arbutus andrachne, A. unedo and their natural hybrid A. × andrachnoides, collected from two different regions in Greece (Kalamos and Varympompi), were analysed comparatively in order to determine their phenolic profile and measure the antioxidant activity using two different single electron transfer-based assays, ferric reducing ability (FRAP) and 2,2-diphenylpicrylhydrazil radical scavenging capacity (DPPH). The pomological characteristics of the hybrid were similar to A. andrachne, while A. unedo had about 2.0-2.5 times larger fruits, with 20% more moisture being 175% heavier. All three species and their biotypes from the two areas had high phenolic content and antioxidant properties and were clearly pulled in different groups. Total flavanols scored a very strong correlation to antioxidant capacity. Highest total flavanols concentrations were found in A. andrachne fruits, while the hybrid had similar concentrations with A. unedo. In samples from Kalamos, concerning condensed tannins, total flavones, flavonols, phenolics and antioxidant capacity FRAP, as well as total anthocyanin and delphinidin 3-O-galactoside, the hybrid presented average values compared to the two parental species, while A. andrachne had the highest values. A strong correlation was found between ortho-diphenols and total soluble solids, as well as of total phenolics and flavonoids with total anthocyanins. The polyphenolic content and the antioxidant capacity varied in different biotypes. A. andrachne biotype from Kalamos showed the highest antioxidant capacity and anthocyanin potential. All A. unedo biotypes and A. × andrachnoides from Varympompi showed higher concentrations of ascorbic acid compared to the other biotypes.

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References

Abidi E, Habib J, Yassine A, Chahine A, Mahjoub T, Elkak A (2015). Effects of methanol extracts from roots, leaves, and fruits of the Lebanese strawberry tree (Arbutus andrachne) on cardiac function together with their antioxidant activity. Pharmaceutical Biology 54:1035-1041. https://doi.org/10.3109/13880209.2015.1100638

Afifi-Yazar FU, Kasabri V, Abu-Dahab R (2011). Medicinal plants from Jordan in the treatment of cancer: traditional uses vs. in vitro and in vivo evaluations-Part 1. Planta Medica 77:1203-1209. http://dx.doi.org/10.1055/s-0030-1270832

Alarcao-E-Silva M, Leitao A, Azinheira H, Leitao M (2001). The arbutus berry: studies on its colour and chemical characteristics at two mature stages. Journal of Food Composition and Analysis 14:27-35. https://doi.org/10.1006/jfca.2000.0962

Arlee R, Suanphairoch, S, Pakdeechanuan P (2013). Differences in chemical components and antioxidant-relatedsubstances in virgin coconut oil from coconut hybrids and their parents. International Food Research Journal 20:2103-2109.

Balasundram N, Sundram K, Samman S (2006). Phenolic compounds in plants and agro-industrial by-products: Antioxidant activity, occurrence, and potential uses. Food Chemistry 99:191-203. https://doi.org/10.1016/j.foodchem.2005.07.042

Barros L, Carvalho AM, Morais JS, Ferreira ICFR (2010). Strawberry-tree, blackthorn and rose fruits: Detailed characterisation in nutrients and phytochemicals with antioxidant properties. Food Chemistry 120:247-254. https://dx.doi.org/10.1016/j.foodchem.2009.10.016

Bertsouklis KF, Papafotiou M (2013). Seed germination of Arbutus unedo, A. andrachne and their natural hybrid A. × andrachnoides in relation to temperature and period of storage. HortScience 48:347-351. https://doi.org/10.21273/HORTSCI.48.3.347

Biniari K, Xenaki M, Daskalakis I, Rusjan D, Bouza D, Stavrakaki M (2020). Polyphenolic compounds and antioxidants of skin and berry grapes of Greek Vitis vinifera cultivars in relation to climate conditions. Food Chemistry 307:125518. https://doi.org/10.1016/j.foodchem.2019.125518

Bisignano G, Tomaino A, Lo Cascio R, Crisalfi G, Uccella N, Saija A (1999). On the in vitro antimicrobial activity of oleuropein and hydroxytyrosol. Journal of Pharmacy and Pharmacology 51:971-974. https://doi.org/10.1211/0022357991773258

Bonvehi JS, Coll FV, Jordà RE (1994). The composition, active components and bacteriostatic activity of propolis in dietetics. Journal of the American Oil Chemists’ Society 71:529-532. https://doi.org/10.1007/BF02540666

Bounous G, Beccaro GL, Mellano MG, Botta R (2009). Nutritional value and antioxidant activity of minor fruits grown in Piemonte (Italy). Acta Horticulturae 818:249-252. https://doi.org/10.17660/ActaHortic.2009.818.36

Caleja C, Barros L, Antonio AL, Oliveira, MBPP, Ferreira ICFR (2017). A comparative study between natural and synthetic antioxidants: Evaluation of their performance after incorporation into biscuits. Food Chemistry 216:342-346. http://dx.doi.org/10.1016/j.foodchem.2016.08.075

Cavaco T, Longuinho C, Quintas C, De Carvalho IS (2007). Chemical and microbial changes during the natural fermentation of strawberry tree (Arbutus unedo L.) fruits. Journal of Food Biochemistry 31:715-725. https://doi.org/10.1111/j.1745-4514.2007.00138.x

Celikel G, Demirsoy L, Demirsoy H (2008). The strawberry tree (A. unedo L.) selection in Turkey. Scientia Horticulturae 118:15-119. https://doi.org/10.1016/j.scienta.2008.05.028

Cervelli C, Farina E, Dalla GC, Giovannini A, Liotta A, Paterniani T, … Aprile S (2012). Development of new ornamental plants and germplasm selection in Mediterranean native species. Acta Horticulturae 937:45-50. https://doi.org/10.17660/ActaHortic.2012.937.3

Dewanto V, Wu X, Adom KK (2002). Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. Journal of Agricultural and Food Chemistry 50:3010-3014. https://doi.org/10.1021/jf0115589

FAO (2010). The contribution of plant genetic resources for food and agriculture to food security and sustainable agricultural development, In: The Second Report on the State of the World’s Plant Genetic Resources for Food and Agriculture. pp 182-201.

Fatin NR, Azrina A (2017). Comparison of vitamin C content in citrus fruits by titration and high-performance liquid chromatography (HPLC) methods. International Food Research Journal Volume 24:726-733.

Flora Europaea (1996). Volume 3. (Tutin TG, HeywoodYH, Burges NA, Moore DM, Valentine DH, Walters S, Weeb DA., Eds). Cambridge University Press, Cambridge, UK.

Fortalezas S, Tavares L, Pimpão R, Tyagi M, Pontes V, Alves PM, … Santos CN (2010). Antioxidant properties and neuroprotective capacity of strawberry tree fruit (Arbutus unedo). Nutrients 2:214-229. https://doi.org/10.3390/nu2020214

Garaguso I, Nardini M (2016). Polyphenols content, phenolics profile and antioxidant activity of organic red wines produced without sulphur dioxide/sulfites addition in comparison to conventional red wines. Food Chemistry 179:336-342. https://doi.org/10.1016/j.foodchem.2015.01.144

Garcia-Alonso M, de Pascual-Teresa S, Santos-Buelga C, Rivas-Gonzalo JC (2004). Evaluation of the antioxidant properties of fruits. Food Chemistry 84:13-18. https://doi.org/10.1016/S0308-8146(03)00160-2

Gazdik Z, Reznicek V, Adam V, Zitka O, Jurikova T, Krska B, … Kizek R (2008). Use of liquid chromatography with electrochemical detection for the determination of antioxidants in less common fruits. Molecules 13:2823-2836. https://dx.doi.org/10.3390%2Fmolecules131102823

González JA, García-Barriuso M, Amich F (2010). Ethnobotanical study of medicinal plants traditionally used in the Arribes del Duero, western Spain. Journal of Ethnopharmacology 131:343-355. https://doi.org/10.1016/j.jep.2010.07.022

Guerreiro AC, Gago CML, Miguel MGC, Antunes MDC (2013). The effect of temperature and film covers on the storage ability of Arbutus unedo L. fresh fruit. Scientia Horticulturae 159:96-102. https://doi.org/10.1016/j.scienta.2013.04.030

Herrera CM (1998). Long-term dynamics of Mediterranean frugivorous birds and fleshy fruits: a 12-year study. Ecological Monographs 68:511-538. https://doi.org/10.1016/j.scienta.2013.04.030

Holubec V, Smekalova T, Paprštein F, Štocková L, Reznícek V (2015). Potential of minor fruit crop wild relatives (CWR) as new crops in breeding for market diversification. In: Redden RJ, Yadav SS, Dulloo ME, Guarino L, Smith P (Eds). Crop wild relatives and climate change. Wiley-Blackwell, USA, pp 293. https://doi.org/10.1002/9781118854396.ch17

Issa RA, Afifi FU, Amro BI (2008). Studying the anti-tyrosinase effect of Arbutus andrachne L. extracts. International Journal of Cosmetic Science 30:271-276. https://doi.org/10.1111/j.1468-2494.2008.00439.x

Koleva II, Niederlander HAG, van Beek TA (2000). An on-line HPLC method for detection of radical scavenging compounds in complex mixtures. Analytical Chemistry 72:2323-2328. https://doi.org/10.1021/ac9912451

Konstantinidis P, Tsiourlis G, Xofis P (2006). Effect of fire season, aspect and pre-fire plant size on the growth of Arbutus unedo L. (strawberry tree) resprouts. Forest Ecology and Management 225:359-367. https://doi.org/10.1016/j.foreco.2006.01.011

Maldini M, D’Urso G, Pagliuca G, Petretto GL, Foddai M, Gallo FR, … Pintore G (2019). HPTLC-PCA Complementary to HRMS-PCA in the case study of Arbutus unedo antioxidant phenolic profiling. Foods 8:294. https://doi.org/10.3390/foods8080294

Mendes L, de Freitas V, Baptista P, Carvalho P (2011). Comparative antihemolytic and radical scavenging activities of strawberry tree (Arbutus unedo L.) leaf and fruit. Food and Chemical Toxicology 49:2285-2291. https://doi.org/10.1016/j.fct.2011.06.028

Mitcham B, Contwell M, Kader A (1996). Methods for determining quality of fresh commodities. Perishable Handling Newsletter Issue 85:1-5

Miguel MG, Faleiro ML, Guerreiro AC, Antunes MD (2014). Arbutus unedo L.: chemical and biological properties. Molecules 19:15799-15823. https://doi.org/10.3390/molecules191015799

Molina M, Pardo-De-Santayana M, Aceituno L, Morales R, Tardío J (2011). Fruit production of strawberry tree (Arbutus unedo L.) in two Spanish forests. Forestry: An International Journal of Forest Research 84:419-429. https://doi.org/10.1093/forestry/cpr031

Morgado S, Morgado M, Plácido AI, Roque F, Duarte AP (2018). Arbutus unedo L.: From traditional medicine to potential uses in modern pharmacotherapy. Journal of Ethnopharmacology 225:90-102. https://doi.org/10.1016/j.jep.2018.07.004

Mosele JI, Macià A, Romero MP, Motilva MJ (2016). Stability and metabolism of Arbutus unedo bioactive compounds (phenolics and antioxidants) under in vitro digestion and colonic fermentation. Food Chemistry 201:120-130. https://doi.org/10.1016/j.foodchem.2016.01.076

Nagata M, Yamashita I (1992). Simple method for simultaneous determination of chlorophyll and carotenoids in tomato fruit. Nippon Shokuhin Kogyo Gakkaishi 39:925-928. https://doi.org/10.3136/nskkk1962.39.925

Ogaya R, Peñuelas J (2007). Species-specific drought effects on flower and fruit production in a Mediterranean holm oak forest. Forestry 80:351-357. https://doi.org/10.1093/forestry/cpm009

Özcan MM, Haciseferoğullari H (2007). The strawberry (Arbutus unedo L.) fruits: Chemical composition, physical properties and mineral contents. Journal of Food Engineering 78:1022-1028. https://doi.org/10.1016/j.jfoodeng.2005.12.014

Pallauf K, Rivas-Gonzalo JC, del Castillo MD, Cano MP, de Pascual-Teresa S (2008). Characterization of the antioxidant composition of strawberry tree (Arbutus unedo L.) fruits. Journal of Food Composition and Analysis 21:273-281. https://doi.org/10.1016/j.jfca.2007.11.006

Papafotiou M, Bertsouklis KF, Trigka M (2013). Micropropagation of Arbutus unedo, A. andrachne, and their natural hybrid A. × andrachnoides, from seedling explants. Journal of Horticultural Science & Biotechnology 88:768-775. https://doi.org/10.1080/14620316.2013.11513037

Papafotiou M, Martini AN (2016). In vitro seed and clonal propagation of the Mediterranean aromatic and medicinal plant Teucrium capitatum. HortScience 51:403-411. https://doi.org/10.21273/HORTSCI.51.4.403

Pasqualone A, Bianco AM, Paradiso VM, Summo C, Gambacorta G, Caponio F, Blanco A (2015). Production and characterization of functional biscuits obtained from purple wheat. Food Chemistry 180:64-70. https://doi.org/10.1016/j.foodchem.2015.02.025

Pavlović RD, Lakusić B, Doslov-Kokorus Z, Kovacević N (2009). Arbutin content and antioxidant activity of some Ericaceae species. Pharmazie 64:656-659. https://doi.org/10.1691/ph.2009.9551

Proloiac A, Raynaud J (1981). Les pigments anthocyaniques des fruits d’ Arbutus unedo L. (Ericacees). Plantes Medicinales et Phytotherapie 15:109-112.

Ruiz-Rodríguez BM, Morales P, Fernández-Ruiz V, Sánchez-Mata MC, Cámara M, Díez-Marqués C, … Tardío J (2011). Valorization of wild strawberry-tree fruits (Arbutus unedo L.) through nutritional assessment and natural production data. Food Research International 44:1244-1253. https://doi.org/10.1016/j.foodres.2010.11.015

Sakar MK, Berkman MZ, Cals I, Ruedύ P (1991). Constituents of Arbutus andrachne. Fitoterapia 62:176-177.

Salem IB, Ouesleti S, Mabrouk Y, Landolsi A, Mouldi S (2018). Exploring the nutraceutical potential and biological activities of Arbutus unedo L. (Ericaceae) fruits. Industrial Crops and products 122:726-731. https://doi.org/10.1016/j.indcrop.2018.06.024

Sansanelli S, Ferri M, Salinitro M, Tassoni A (2017). Ethnobotanical survey of wild food plants traditionally collected and consumed in the Middle Agri Valley (Basilicata region, southern Italy). Journal of ethnobiology and ethnomedicine 13:50. https://doi.org/10.1186/s13002-017-0177-4

Sarneckis C, Dambergs R, Jones P, Mercurio MD, Herderich MJ, Smith PA (2006). Quantification of condensed tannins by precipitation with methyl cellulose: Development and validation of an optimized tool for grape and wine analysis. Australian Journal of Grape and Wine Research 12:39-49. https://doi.org/10.1111/j.1755-0238.2006.tb00042.x

Seker M, Toplu C (2010). Determination and comparison of chemical characteristics of Arbutus unedo L. and Arbutus andrachne L. (family Ericaceae) fruits. Journal of Medicinal Food 13:1013-1018. https://doi.org/10.1089/jmf.2009.0167

Serçe S, Özgen M, Torun AA, Ercisli S (2010). Chemical composition, antioxidant activities and total phenolic content of Arbutus andrachne L. (Fam. Ericaceae) (the Greek strawberry tree) fruits from Turkey. Journal of Food Composition and Analysis 23:619-623. https://doi.org/10.1016/j.jfca.2009.12.007

Somers TC, Evans ME (1977). Spectral evaluation of young red wines: anthocyanin equilibria, total phenolic, free and molecular SO2, ‘chemical age’. Journal of the Science of Food and Agriculture 28:279-287. http://refhub.elsevier.com/S0308-8146(19)31636-X/h0170

Soobrattee MA, Neergheen VS, Luximon-Ramma A, Aruoma OI, Bahorun T (2005). Phenolics as potential antioxidant therapeutic agents: mechanism and actions. Mutation Research 579:200-213. https://doi.org/10.1016/j.mrfmmm.2005.03.023

Souci SW, Fachmann W, Kraut H (2008). Food composition and nutrition tables (7rd ed). Stuttgart: Med pharm Scientific Publishers.

Soufleros EH, Mygdalia SA, Natskoulis P (2005). Production process and Characterization of the traditional Greek fruit distillate “Koumaro” by aromatic and mineral composition. Journal of Food Composition and Analysis 18:699-716. https://doi.org/10.1016/j.jfca.2004.06.010

Sulusoglu M, Cavusoglu A, Erkal S (2011). Arbutus unedo L. (Strawberry tree) selection in Turkey Samanli Mountain locations. Journal of Medicinal Plants Research 5:3545-3551.

Tenuta MC, Tundis R, Xiao J, Loizzo MR, Dugay A, Deguin B (2018). Arbutus species (Ericaceae) as source of valuable bioactive products. Critical Reviews in Food Science and Nutrition 59:864-881. https://doi.org/10.1080/10408398.2018.1551777

Tsuda T, Ueno Y, Yoshikawa T, Kojo H, Osawa T (2006). Microarray profiling of gene expression in human adipocytes in response to anthocyanins. Biochemical Pharmacology 71:1184-1197. https://doi.org /10.1016/j.bcp.2005.12.042

Tuberoso CIG, Bifulco E, Caboni P, Cottiglia F, Cabras P, Floris I (2010). Floral markers of strawberry tree (Arbutus unedo L.) honey. Journal of Agricultural and Food Chemistry 58:384-389. https://doi.org/10.1021/jf9024147

Vattem DA, Shetty K (2005). Biological functionality of ellagic acid: A review. Journal of Food Biochemistry 29:234-266. https://doi.org/10.1111/j.1745-4514.2005.00031.x

Vivas N, Glories Y, Lagune L, Saucier C, Augustin M (1994). Estimation du degré de polymerisation des procyanidins du raisin et du vin par la méthode au dimethylaminocinnamaldehyde. Journal International des Sciences de la Vigne et du Vin 28:319-336. https://doi.org/10.20870/oeno-one.1994.28.4.1138

Vlachou G, Papafotiou Μ, Bertsouklis KF (2019). Studies on seed germination and micropropagation of Clinopodium nepeta a medicinal and aromatic plant. HortScience 54:1558-1564. https://doi.org/10.21273/HORTSCI13996-19

Xu C, Zhang Y, Cao L, Lu J (2010). Phenolic compounds and antioxidant properties of different grape cultivars grown in China. Food Chemistry 119:1557-1565. https://doi.org/10.1016/j.foodchem.2009.09.042

Published
2021-02-15
How to Cite
BERTSOUKLIS, K. F., DASKALAKIS, I., BINIARI, K., & PAPAFOTIOU, M. (2021). Comparative study of polyphenolic content and antioxidant capacity in fruits of Arbutus unedo, A. andrachne and their natural hybrid A.× andrachnoides. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(1), 12165. https://doi.org/10.15835/nbha49112165
Section
Research Articles
CITATION
DOI: 10.15835/nbha49112165