Abstract
Apple is a fruit that is frequently consumed in daily diet and is very useful for human health. In this study, seven apple cultivars grown in Posof district in Ardahan province, including red-fleshed ‘İçi Kırmızı’ and ’Japon apples’ were investigated. ’Japon apple’ was found to have the highest values of total phenolic and ascorbic acid contents. The highest content of chlorophyll a (1.14 μg/g) was measured in ‘Mahara apple’, while the highest contents of chlorophyll b and total carotenoids (1.22 and 0.70 μg/g, respectively) were also observed in ‘Japon apple’. All the fruits and leaves of the apple cultivars, used in this study exhibited differential antioxidant and antibacterial effects. Except for ‘Şeker apple’, all methanolic leaf extracts exhibited inhibitory effects on Saccharomyces cerevisiae. In addition, the strongest antimicrobial activities were observed in ‘Japon apple’. While none of the doses of aqueous fruit extracts showed antimutagenic activities, different doses of the methanolic leaf extracts of the samples exhibited antimutagenic effects.
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18 November 2020
An Erratum to this paper has been published: https://doi.org/10.1007/s10341-020-00532-8
References
Agourram A, Ghirardello D, Rantsiou K, Zeppa G, Belviso S, Romane A, Oufdou K, Giordano M (2013) Phenolic content, antioxidant potential and antimicrobial activities of fruit and vegetable by-product extracts. Int J Food Prop 16:1092–1104. https://doi.org/10.1080/10942912.2011.576446
Ahmad N, Mukhtar H (1999) Green tea polyphenols and cancer: Biologic mechanisms and practical implications. Nutr Rev 57:78–83. https://doi.org/10.1111/j.1753-4887.1999.tb06927.x
AOAC (1990) Official methods of analysis of the association of official analytical chemists, 15th edn., pp 1058–1059
Bakhshi D, Arakawa O (2006) Effects of UV‑b irradiation on phenolic compound accumulation and antioxidant activity in ‘Jonathan’ apple influenced by bagging, temperature and maturation. J Food Agr Environ 4(1):75–79. https://doi.org/10.1234/4.2006.698
Benzie IFF, Strain JJ (1996) The ferric reducing Ability of plasma (FRAB) as a measure of “Antioxidant power”: The FRAB assay. Anal Biochem 239:70–76. https://doi.org/10.1006/abio.1996.0292
Bradshaw LJ (1992) Laboratory microbiology. 4th edn., Saunders College Publishing, Harcourt Brace Javanovich College Publisher, New York
Cemeroğlu B (1992) Meyve ve sebze işleme endüstrisinde temel analiz metotları. Biltav Yayınları, Ankara
Chiang BT, Nakhla MK, Maxwell DP, Schoenfelder M, Green SK (1997) A new geminivirus associated with a leaf curl disease of tomato in Tanzani. Plant Dis 81:111. https://doi.org/10.1094/PDIS.1997.81.1.111B
Ciocan ID, Bára I (2007) Plant products as antimicrobial agents. Universitatii Ale Ştiintifice Analele Alexandru Ioan Cuza, Secţiunea Genetică şi Biologie Moleculară, TOM VIII, 151–156
Collins CM, Lyne PM, Grange JM (1989) Antimicrobial sensitivity and assay tests. Collins and Lyne’s microbiological methods. Butterworths, London
Cueva C, Moreno-Arribas M, Martín-Álvarez PJ, Bills G, Vicente MF, Basilio A, Rivas CL, Requena T, Rodriquez JM, Bartolome B (2010) Antimicrobial activity of phenolic acids against commensal, probiotic and pathogenic bacteria. Res Microbiol 161:372–382. https://doi.org/10.1016/j.resmic.2010.04.006
Davey MW, Van Montagu M, Inze D, Sanmartin M, Kanellis A, Smirnoff N, Benzie I, Strain J, Favell D, Fletcher J (2000) Plant L‑ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. J Sci Food Agric 80:825–860. https://doi.org/10.1002/(SICI)1097-0010(20000515)80:7〈825::AID-JSFA598〉3.0.CO;2‑6
Davies KM (2009) Modifying anthocyanin production in flowers. In: Gould K, Davies K, Winefield C (eds) Anthocyanins: biosynthesis function and applications. Springer, New York, pp 471–552
Davis PH (1984) Flora of Turkey and east Aegean islands. Edinburgh University Press, Edinburgh
De-Kok L, Graham M (1989) Levels of pigments, soluble proteins, amino acids and sulfhydryl compounds in foliar tissue of Arabidobsis thaliana during dark induced and natural senescence. Plant Physiol Biochem 27:203–209
Dowdle J, Ishikawa T, Gatzek S, Rolinski S, Smirnoff N (2007) Two genes in arabidopsis thaliana encoding GDP-L-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. Plant J 52:673–689. https://doi.org/10.1111/j.1365-313X.2007.03266.x
Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42. https://doi.org/10.2307/3001478
Dziubiak M (2004) Collection of the genus Malus Mill. in the botanical garden of the polish Academy of sciences in Warsaw. J Fruit Ornam Plant Res 12:121–128
Ercişli S (2004) A short review of the fruit germplasm resources of Turkey. Genet Resour Crop Ev 51:419–435. https://doi.org/10.1023/B:GRES.0000023458.60138.79
Feliciano RP, Antunes C, Ramos A, Serra AT, Figueira ME, Duarte CMM, de Carvalho A, Bronze MR (2010) Characterization of traditional and exotic apple varieties from Portugal. Part 1—Nutritional, phytochemical and sensory analysis. J Funct Foods 2:35–45. https://doi.org/10.1016/j.jff.2009.12.004
Giusti MM, Wrolstad RE (2001) Characterization and measurement of anthocyanins by UV-visible spectroscopy. Curr Protoc Food Anal Chem. https://doi.org/10.1002/0471142913.faf0102s00
Hatier JHB, Gould KS (2009) Anthocyanin function in vegetative organs. In: Gould K, Davies K, Winefield C (eds) Anthocyanins: biosynthesis functions and applications. Springer, New York, pp 1–20
Hayek SA, Gyawali R, Ibrahim SA (2013) Antimicrobial natural products. In: Méndez-Vilas A (ed) Microbial pathogens and strategies for combating them, Science, technology and education, pp 910–921
Holiman PCH, Hertog MGL, Katan MB (1996) Analysis and health effects of flavonoids. Food Chem 57:43–46. https://doi.org/10.1016/0308-8146(96)00065-9
Hughes NM, Neufeld HS, Burkey KO (2005) Functional role of anthocyanins in high-light winter leaves of the evergreen herb Galax urceolata. New Phytol 168:575–587. https://doi.org/10.1111/j.1469-8137.2005.01546.x
Jelodarian S, Ebrahimabadi AH, Kashi FJ (2013) Evoluation of antimicrobial activity of Malus domestica fruit extract from Kashan area. Avicenna J Phytomed 3:1–6
Jeong MR, Kim HY, Cha JD (2009) Antimicrobial activity of methanol extract from Ficus carica leaves against oral bacteria. J Bacteriol Virol 39:97–102. https://doi.org/10.4167/jbv.2009.39.2.97
Lai P, Roy J (2004) Antimicrobial and chemopreventive properties of herbs and spices. Curr Med Chem 11:1451–1460. https://doi.org/10.2174/0929867043365107
Leal-Cardoso JH, Fonteles MC (1999) Pharmacological effects of essential oils of plants of the northeast of Brazil. An Acad Bras Cienc 71:207–213
Ma FW, Cheng LL (2003) The sun-exposed peel of apple fruit has higher xanthophyll cycle-dependent thermal dissipation and antioxidants of the ascorbate–glutathione pathway than the shade peel. Plant Sci 165:819–827. https://doi.org/10.1016/S0168-9452(03)00277-2
Maron DM, Ames BN (1983) Revised methods for the Salmonella mutagenicity test. Mutat Res 113:173–215. https://doi.org/10.1016/0165-1161(83)90010-9
Nakamura CV, Ueda-Nakamura T, Bando E, Melo AF, Cortz DA, Dias Filha BP (1999) Antibacterial Activity of Ocimum gratissimum L. Essential Oil. Mem Inst Oswaldo Cruz 94:675–678. https://doi.org/10.1590/S0074-02761999000500022
Neill SO, Gould KS (2003) Anthocyanins in leaves: light attenuators or antioxidants? Funct Plant Biol 30:865–873. https://doi.org/10.1071/FP03118
Neill S, Gould KS, Kilmartin PA, Mitchell KA, Markham KR (2002) Antioxidant capacities of green and cyanic leaves in the sun species Quintinia serrata. Funct Plant Biol 29:1437–1443. https://doi.org/10.1071/FP02100
van Nocker S, Berry G, Najdowski J, Michelutti R, Luffman M, Forsline P, Alsmairat N, Beaudry R, Nair MG, Ordidge M (2012) Genetic diversity of red-fleshed apples (Malus). Euphytica 185:281–293. https://doi.org/10.1007/s10681-011-0579-7
Qu YH, Xu GX, Zhou JZ, Chen TD, Zhu LF, Shields PG, Wang HW, Gao YT (1992) Genotoxicity of heated cooking oil vapors. Mutat Res 298:105–111. https://doi.org/10.1016/0165-1218(92)90035-X
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. https://doi.org/10.1016/S0891-5849(98)00315-3
Rezaeirad D, Bakhshi D, Ghasemnezhad M, Lahiji HS (2013) Evaluation of some quantitative and qualitative characteristics of local pears (Pyrus sp.) in the North of Iran. Int J Agr Crop Sci 5:882–887
Rubnov S, Kashman Y, Rabinowitz R, Schlesinger M, Mechoulam R (2001) Suppressors of cancer cell proliferation from fig (Ficus carica) resin: isolation and structure elucidation. J Nat Prod 64:993–996. https://doi.org/10.1021/np000592z
Ryu SR, Cho H, Jung JS, Jung ST (1998) The study on the separation and antitumor activity as new substances in fig. J Applied Chem 2:961–964
Sadik CD, Sies H, Schewe T (2003) Inhibition of 15-lipoxygenases by flavonoids: structure activity relations and mode of action. Biochem Pharmacol 65:773–781. https://doi.org/10.1016/S0006-2952(02)01621-0
Savoia D (2012) Plant-derived antimicrobial compounds: alternatives to antibiotics. Future Microbiol 7:979–990. https://doi.org/10.2217/fmb.12.68
Şarer E (1991) Uçucu yağların biyolojik etkileri ve tedavide kullanımları. 9. Bitkisel ilaç hammaddeleri toplantısı, Eskişehir
Shao L, Shu Z, Sun SH, Peng CH, Wang X, Lin ZH (2007) Antioxidation of anthocyanins in photosynthesis under high temperature stres. J Integr Plant Biol 49:1341–1351. https://doi.org/10.1111/j.1744-7909.2007.00527.x
Spanos GA, Wrolstad RE (1992) Phenolic of apple, pear and white grape juices and their changes with processing and storage. J Agric Food Chem 40:1478–1487. https://doi.org/10.1021/jf00021a002
Steyn WJ (2009) Prevalance and functions of anthociyanins in fruits. In: Gould K, Davies K, Winefield C (eds) Anthocyanins: biosynthesis functions and applications. Springer, New York, pp 85–105
Stojković D, Petrović J, Soković M, Glamočlija J, Kukić-Marković J, Petrović S (2013) In situ antioxidant and antimicrobial activities of naturally occurring caffeic acid, p‑coumaric acid and rutin, using food systems. J Sci Food Agric 93(13):3205–3208. https://doi.org/10.1002/jsfa.6156
Vaya J, Mahmood S (2006) Flavonoid content in leaf extracts of the fig (Ficus carica L.), carob (Ceratonia siliqua L.) and pistachio (Pistacia lentiscus L.). Biofactors 28:169–175. https://doi.org/10.1002/biof.5520280303
Vieira FGK, Borges GSC, Copetti C, Gonzaga LV, Nunes EC, Fett R (2009) Activity and contents of polyphenolic antioxidants in the whole fruit, flesh and peel of three apple cultivars. Arch Latinoam Nutr 59:101–106
Vrhovsek U, Rigo A, Tonon D, Mattivi F (2004) Quantification of polyphenols in different apple varieties. J Agr Food Chem 52:6532–6538. https://doi.org/10.1021/jf049317z
Walia M, Mann TS, Kumar D, Agnihotri VK, Singh B (2012) Chemical composition and in vitro cytotoxic activity of essential oil of leaves of Malus domestica Growing in Western Himalaya (India). Evid Based Complement Alternat Med. https://doi.org/10.1155/2012/649727
Wiseman A (2003) Biologically‐active phytochemicals in food: analysis, metabolism, bioavailability and function Edited by W Pfannhauser, GR Fenwick and S Khokhar Royal Society of Chemistry, Cambridge, 2001 pp 616, ISBN 0‐85404‐806‐5. J Sci Food Agric 83:866. https://doi.org/10.1002/jsfa.1328
Wolfe KL, Liu RH (2002) Apple peels are rich in phytochemicals and have high antioxidant activity. Fruit Q 10:9–11
Wolfe KL, Liu RH (2003) Apple peels as a value-added food ingredient. J Agr Food Chem 51:1676–1683. https://doi.org/10.1021/jf025916z
Wolfe KL, Wu X, Liu RH (2003) Antioxidant activity of apple peels. J Agric Food Chem 51:609–614. https://doi.org/10.1021/jf020782a
Yabuta Y, Mieda T, Rapolu M, Nakamura A, Motoki T, Maruta T, Yoshimura K, Ishikawa T, Shigeoka S (2007) Light regulation of ascorbate biosynthesis is dependent on the photosynthetic electron transport chain but independent of sugars in Arabidopsis. J Exp Bot 58:2661–2671. https://doi.org/10.1093/jxb/erm124
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We thank The Scientific and Technological Research Council of Turkey (TUBITAK) for supporting our study through Project Grants No. 115Z833.
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N. Erbil, M. Arslan, Z.T. Murathan, A. Ilcim and B. Sayin Borekci declare that they have no competing interests.
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The original online version of this article was revised: The address of Bilge Sayin Borekci was incorrect and the acknowledgement was missing. Full information regarding the corrections made can be found in the erratum for this article.
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Erbil, N., Arslan, M., Murathan, Z.T. et al. Some Biological Effects of the Fruits and Leaves of Different Apple Cultivars, Including Red-Fleshed Apples, Grown in a Microclimatic Region of Turkey: Part I. Erwerbs-Obstbau 62, 399–410 (2020). https://doi.org/10.1007/s10341-020-00527-5
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DOI: https://doi.org/10.1007/s10341-020-00527-5