ESTONIAN ACADEMY
PUBLISHERS
eesti teaduste
akadeemia kirjastus
PUBLISHED
SINCE 1952
 
Proceeding cover
proceedings
of the estonian academy of sciences
ISSN 1736-7530 (Electronic)
ISSN 1736-6046 (Print)
Impact Factor (2022): 0.9
Research article
Polyphenolic compounds in apple (Malus domestica Borkh.) cultivars grown in Estonia; pp. 154–166
PDF | https://doi.org/10.3176/proc.2023.2.06

Authors
Karmen Kapp, Kaisa Kalder, Ave Kikas, Toivo Univer, Tõnu Püssa, Ain Raal
Abstract

Several studies have shown that apples (Malus domestica Borkh.) in the daily diet are healthy due to their rich content of phytochemicals. The aim of this study was to compare the content of polyphenols in the peels, flesh, seeds and leaves of five apple cultivars (‘Antonovka’, ‘Åkerö’, ‘Cortland’, ‘Karksi renett’ and ‘Krista’) grown in Estonia. Of the 21 collected cultivars, these five were selected on the basis of their rich or distinct chemical composition according to the LC-DAD-MS/MS data. In addition, the weight of the fruit, the number of seeds in the fruit and the weight of the seeds were determined. A total of 33 compounds were detected in the peels, 23 in the flesh, 11 in the seeds, and 25 in the leaves. They belong to four groups: 1) flavon-3-ols (quercetin and its derivatives), 2) dihydrochalcones (phloretin and its derivatives), 3) flavan-3-ols (catechin, epicatechin and oligomers), and 4) esters formed between caffeic acid and L-quinic acid (chlorogenic acid). Based on the data presented in this article, the leaves contained the highest measured total polyphenol content (TPGA). The peels contained high amounts of all the major polyphenolic groups mentioned. The apple flesh lacked flavon-3-ols and the seeds flavon-3-ols and flavan-3-ols. In the peels, the major polyphenols were quercetin galactoside (3–342 mg/100 g), procyanidin B1 (18–179 mg/100 g), and (epi)catechin trimer (28–200 mg/100 g); in the flesh chlorogenic acid (77–298 mg/100 g); in the seeds phloridzin (466 mg/100 g in ‘Cortland’); and in the leaves chlorogenic acid (147–446 mg/100 g) and quercetin glycosides, especially quercetin rhamnoside (242–350 mg/100 g), quercetin galactoside (39–334 mg/100 g) and quercetin glucoside (91–321 mg/100 g).

References

Bergmann, C. B., McReynolds, C. B., Wan, D., Singh, N., Goetzman, H., Caldwell, C. C. et al. 2022. sEH-derived metabolites of linoleic acid drive pathologic inflammation while impairing key innate immune cell function in burn injury. Proc. Natl. Acad. Sci.119(13), e2120691119.
https://doi.org/10.1073/pnas.2120691119

Boyer, J. and Liu, R. H. 2004. Apple phytochemicals and their health benefits. Nutr. J.3(5), 174–185.
https://doi.org/10.1186/1475-2891-3-5

Buccheri, M. and Di Vaio, C. 2004. Relationship among seed number, quality, and calcium content in apple fruits. J. Plant Nutr., 27(10), 1735–1746. 
https://doi.org/10.1081/PLN-200026409

Chen, J., Zhang, H., Hu, X., Xu, M., Su, Y., Zhang, C. et al.  2022. Phloretin exhibits potential food-drug interactions by inhibiting human UDP-glucuronosyltransferases in vitro. Toxicol. Vitro84, 105447. 
https://doi.org/10.1016/j.tiv.2022.105447

Drogoudi, P. D., Michailidis, Z. and Pantelidis, G. 2008. Peel and flesh antioxidant content and harvest quality char­acteristics of seven apple cultivars. Sci. Hortic., 115, 149– 153.
https://doi.org/10.1016/j.scienta.2007.08.010

Duda-Chodak, A., Tarko, T. and Tuszyński, T. 2011. Antioxidant activity of apples – an impact of maturity stage and fruit part. Acta Sci. Pol. Technol. Aliment.,10(4), 443–454.

Eslon, J., Jaama, A. and Siimon, A. 1970. Eesti pomoloogia (Estonian Pomology). Valgus, Tallinn (in Estonian).

Fromm, M., Bayha, S., Carle, R. and Kammerer, D. R. 2012. Characterization and quantitation of low and high molecular weight phenolic compounds in apple seeds. J. Agric. Food Chem.60, 1232–1242.
https://doi.org/10.1021/jf204623d

Fruit Genetic Resources of Estonian University of Life Sciences.
https://sordivaramu.emu.ee/kategooria.php?lang=gb&id=&mis=ounviljalised (accessed 2022-11-11).

Gabbs, M., Leng, S., Devassy, J. G., Monirujjaman, M. and Aukema, H. M. 2015. Advances in our understanding of oxyli­pins derived from dietary PUFAs. Adv. Nutr.6(5), 513–540.
https://doi.org/10.3945/an.114.007732

Gao, S. S., Chen, X. Y., Zhu, R. Z., Choi, B.-M., Kim, S. J. and Kim, B.-R. 2012. Dual effects of phloretin on aflatoxin B1 metabolism: activation and detoxification of aflatoxin B1. Biofactors38, 34–43. 
https://doi.org/10.1002/biof.190

Garkava-Gustavsson, L., Mujaju, C., Sehic, J., Zborowska, A., Backes, G. M., Hietaranta, T. and Antonius, K. 2013. Gen­etic diversity in Swedish and Finnish heirloom apple cul­- tivars revealed with SSR markers. Sci. Hortic.162, 43–48.
https://doi.org/10.1016/j.scienta.2013.07.040

Gharghani, A., Zamani, Z., Talaie, A., Oraguzie, N. C., Fatahi, R., Hajnajari, H. et al.  2009. Genetic identity and relationships of Iranian apple (Malus × domestica Borkh.) cultivars and landraces, wild Malus species and representative old apple cultivars based on simple sequence repeat (SSR) marker analysis. Genet. Resour. Crop Evol.56, 829–842.
https://doi.org/10.1007/s10722-008-9404-0

Hampson, C. R. and Quamme, H. A. 2000. Use of preference testing to identify tolerance limits for fruit visual attributes in apple breeding. HortScience35(5), 921–924.
https://doi.org/10.21273/HORTSCI.35.5.921

Herregods, M. 1999. Profitable quality: Cost and profits con­cerning marketing. A product preferred by consumer. In Post-Harvest Losses of Perishable Horticultural Products in the Mediterranean Region (Gerasopoulos, D., ed.). CIHEAM, Chania, 11–18. 

Hyson, D. A. 2011. A comprehensive review of apples and apple components and their relationship to human health. Adv. Nutr., 2(5), 408–420.
https://doi.org/10.3945/an.111.000513

Jaagus, J. 1997. The impact of climate change on the snow cover pattern in Estonia. Clim. Change36(1–2), 65–77.
https://doi.org/10.1023/A:1005304720412

Jakobek, L., García-Villalba, R. and Tomás-Barberán, F. A. 2013. Polyphenolic characterization of old local apple varieties from Southeastern European region. J. Food Compos. Anal.31(2), 199–211.
https://doi.org/10.1016/j.jfca.2013.05.012

Kask, K. 2010. Puuviljandus Eestis. Sordid ja aretajad (Horticulture in Estonia. Cultivars and Breeders). Estonian University of Life Sciences, Tartu (in Estonian).

Kask, K. and Kivistik, J. 2005. Puuviljad ja marjad Eestis (Fruits and Berries in Estonia). Kirjastus Ilo, Tallinn (in Estonian).

Kask, K., Jänes, H., Libek, A., Arus, L., Kikas, A., Kaldmäe, H. et al. 2010. New cultivars and future perspectives in professional fruit breeding in Estonia. Agron. Res.(Special Issue III), 603–614. 

Kimura, Y., Ito, H., Ohnishi, R. and Hatano, T. 2010. Inhibitory effects of polyphenols on human cytochrome P450 3A4 and 2C9 activity. Food Chem. Toxicol.48(1), 429–435.
https://doi.org/10.1016/j.fct.2009.10.041

Kondo, S., Tsuda, K., Muto, N. and Ueda, J. 2002. Antioxidative activity of apple skin or flesh extracts associated with fruit development on selected apple cultivars. Sci. Hortic., 96, 177–185.
https://doi.org/10.1016/S0304-4238(02)00127-9

Kviklys, D., Kviklienė, N., Bite, A., Lepsis, J., Univer, T., Univer, N. et al. 2012. Baltic fruit rootstock studies: evaluation of 12 apple rootstocks in North-East Europe. Hortic. Sci.39(1), 1–7.
https://doi.org/10.17221/29/2011-HORTSCI

Kviklys, D., Viškelis, J., Liaudanskas, M., Janulis, V., Laužikė, K., Samuolienė, G. et al. 2022. Apple fruit growth and quality depend on the position in the tree canopy. Plants11, 196.
https://doi.org/10.3390/plants11020196

Lata, B., Trampczynska, A. and Paczesna, J. 2009. Cultivar variation in apple peel and whole fruit phenolic composition. Sci. Hortic.121(2), 176–181.
https://doi.org/10.1016/j.scienta.2009.01.038

Lee, K. W., Kim, Y. J., Kim, D.-O., Lee, H. J. and Lee, C. Y. 2003. Major phenolics in apple and their contribution to the total antioxidant capacity. J. Agric. Food Chem.51(22), 6516–6520.
https://doi.org/10.1021/jf034475w

Liaudanskas, M., Zymone, K., Viskelis, J., Kviklys, D., Viskelis, P. and Janulis, V. 2018. Seasonal variation of the qualitative and quantitative composition of phenolic compounds in Malus domestica leaves. Chem. Nat. Compd.54, 348–349.
https://doi.org/10.1007/s10600-018-2341-z

Luckwill, L. C., Weaver, P. and MacMillan, J. 1969. Gibberellins and other growth hormones in apple seeds. J. Hortic. Sci.44, 413–124.
https://doi.org/10.1080/00221589.1969.11514325

Mägi, E. 1975. Õunapuu (Apple Tree). Valgus, Tallinn (in Estonian).

Mainla, L., Moor, U., Karp, K. and Püssa, T. 2011. The effect of genotype and rootstock on polyphenol composition of selected apple cultivars in Estonia. Žemdirbystė-Agric.98(1), 63–70.

Marcotte, B. V., Verheyde, M., Pomerleau, S., Doyen, A. and Couillard, C. 2022. Health benefits of apple juice con­sumption: a review of interventional trials on humans. Nutrients14(4), 821.
https://doi.org/10.3390/nu14040821

Markaverich, B. M., Alejandro, M., Thompson, T., Mani, S., Reyna, A., Portillo, W. et al. 2007. Tetrahydrofurandiols (THF-diols), leukotoxindiols (LTX-diols), and endocrine disruption in rats. Environ. Health Perspect., 115(5), 702–708. 
https://doi.org/10.1289/ehp.9311

Masumoto, S., Terao, A., Yamamoto, Y., Mukai, T., Miura, T. and Shoji, T. 2016. Non-absorbable apple procyanidins prevent obesity associated with gut microbial and metabolomic changes. Sci. Rep., 6, 31208.
https://doi.org/10.1038/srep31208

McGhie, T. K., Hunt, M. and Barnet, L. E. 2005. Cultivar and growing region determine the antioxidant polyphenolic concentration and composition of apples grown in New Zealand. J. Agric. Food Chem.53(8), 3065–3070.
https://doi.org/10.1021/jf047832r

Monfoulet, L.-E., Buffière, C., Istas, G., Dufour, C., Le Bourvellec, C., Mercier, S. et al. 2020. Effects of the apple matrix on the postprandial bioavailability of flavan-3-ols and nutrigenomic response of apple polyphenols in mini­pigs challenged with a high fat meal. Food Funct., 11(6), 5077–5090.
https://doi.org/10.1039/D0FO00346H

Napolitano, A., Cascone, A., Graziani, G., Ferracane, R., Scalfi, L., Di Vaio, C. et al. 2004. Influence of variety and storage on the polyphenol composition of apple flesh, J. Agric. Food Chem., 52(21), 6526–6531.
https://doi.org/10.1021/jf049822w

Nguyen, N. A., Cao, N. T., Nguyen, T. H. H., Le, T.-K., Cha, G. S., Choi, S.-K. et al.  2020. Regioselective hydroxylation of phloretin, a bioactive compound from apples, by human cytochrome P450 enzymes. Pharmaceuticals13(11), 330. 
https://doi.org/10.3390/ph13110330

Nie, Y., Ren, D., Lu, X., Sun, Y. and Yang, X. 2015. Differential protective effects of polyphenol extracts from apple peels and fleshes against acute CCl4-induced liver damage in mice. Food Funct., 6(2), 513–524.
https://doi.org/10.1039/C4FO00557K

Ogino, Y., Osada, K., Nakamura, S, Ohta, Y., Kanda, T. and Sugano, M. 2007. Absorption of dietary cholesterol oxidation products and their downstream metabolic effects are reducted by dietary apple polyphenols. Lipids42(2), 151–161.
https://doi.org/10.1007/s11745-006-3008-2

Petkovšek, M. M., Stampar, F. and Veberic, R. 2007. Parameters of inner quality of the apple scab resistant and susceptible apple cultivars (Malus domesticaBorkh.). Sci. Hortic., 114(1), 37–44.
https://doi.org/10.1016/j.scienta.2007.05.004

Petkovšek, M. M., Stampar, F. and Veberic, R. 2008. Increased phenolic content in apple leaves infected with the apple scab pathogen. J. Plant Pathol.90(1), 49–55.

Petkovšek, M. M., Slatnar, A., Stampar, F. and Veberic, R. 2011. Phenolic compounds in apple leaves after infection with apple scab. Biol. Plant.55(4), 725–730.
https://doi.org/10.1007/s10535-011-0176-6

Picinelli, A., Dapena, E. and Mangas, J. J. 1995. Polyphenolic pattern in apple tree leaves in relation to scab resistance. A preliminary study. J. Agric. Food Chem., 43(8), 2273–2278.
https://doi.org/10.1021/jf00056a057

Pohl, C., Will, F., Dietrich, H. and Schrenk, D. 2006. Cytochrome P450 1A1 expression and activity in Caco-2 cells: modulation by apple juice extract and certain apple polyphenols. J. Agric. Food Chem.54(26), 10262–10268. 
https://doi.org/10.1021/jf061791c

Renard, C. M. G. C., Dupont, N. and Guillermin, P. 2007. Concentrations and characteristics of procyanidins and other phenolics in apple during fruit growth. Phytochemistry68, 1128–1138.
https://doi.org/10.1016/j.phytochem.2007.02.012

Seppä, L. 2014. Domestic apple cultivars: sensory descriptions and consumer responses.  Doctoral dissertation. University of Helsinki, Helsinki.

Serra, A. T., Rocha, J., Sepodes, B., Matias, A. A., Feliciano, R. P., de Carvalho, A. et al. 2012. Evaluation of cardiovascular protective effect of different apple variates – correlation of response with composition. Food Chem., 135(4), 2378–2386. 
https://doi.org/10.1016/j.foodchem.2012.07.067

Sun, J. and Liu, R. H. 2008. Apple phytochemical extracts inhibit proliferation of estrogen-dependent and estrogen-indepen­dent human breast cancer cells through cell cycle modu- lation. J. Agric. Food Chem.56(24), 11661–11667.
https://doi.org/10.1021/jf8021223

Tahir, I. I., Johansson, E. and Olsson, M. E. 2007. Improvement of quality and storability of apple cv. Aroma by adjustment of some pre-harvest conditions. Sci. Hortic., 112(2), 164–171.
https://doi.org/10.1016/j.scienta.2006.12.018

Toom, M., Talgre, L., Mäe, A., Tamm, S., Narits, L., Edesi, L. et al. 2019. Selecting winter cover crop species for northern climatic conditions. Biol. Agric. Hortic.35(4), 263–274.
https://doi.org/10.1080/01448765.2019.1627908

Treutter, D. 2001. Biosynthesis of phenolic compounds and its regulation in apple. Plant Growth Regul., 34, 71–89.
https://doi.org/10.1023/A:1013378702940

Tsao, R., Yang, R., Young, J. C. and Zhu, H. 2003. Polyphenolic profiles in eight apple cultivars using high-performance liquid chromatography (HPLC). J. Agric. Food Chem.51(21)6347–6353.
https://doi.org/10.1021/jf0346298

Veberic, R., Trobec, M., Herbinger, K., Hofer, M., Grill, D. and Stampar, F. 2005. Phenolic compounds in some apple (Malus domestica Borkh.) cultivars of organic and integrated production. J. Sci. Food Agric.85(10), 1687–1694.
https://doi.org/10.1002/jsfa.2113

Warrington, I. J., Fulton, T. A., Halligan, E. A. and de Silva, H. N. 1999. Apple fruit growth and maturity are affected by early season temperatures. J. Am. Soc. Hortic. Sci.124(5), 468–477.
https://doi.org/10.21273/JASHS.124.5.468

Wojdyło, A. and Oszmiański, J. 2020. Antioxidant activity modu­lated by polyphenol contents in apple and leaves during fruit development and ripening. Antioxidants9(7), 567.
https://doi.org/10.3390/antiox9070567

Wu, J., Gao, H., Zhao, L., Liao, X., Chen, F., Wang, Z. and Hu, X. 2007. Chemical compositional characterization of some apple cultivars. Food Chem.,103(1), 88–93.
https://doi.org/10.1016/j.foodchem.2006.07.030

Xu, Y., Fan, M., Ran, J., Zhang, T., Sun, H., Dong, M. et al. 2016. Variation in phenolic compounds and antioxidant activity in apple seeds of seven cultivars. Saudi J. Biol. Sci.23(3), 379–388.
https://doi.org/10.1016/j.sjbs.2015.04.002

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