Phenolic compounds in some apple (Malus domestica Borkh) cultivars of organic and integrated production
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1 Journal of the Science of Food and Agriculture J Sci Food Agric 85: (2005) DOI: /jsfa.2113 Phenolic compounds in some apple (Malus domestica Borkh) cultivars of organic and integrated production Robert Veberic, 1 Mateja Trobec, 1 Karin Herbinger, 2 Melanie Hofer, 2 Dieter Grill 2 and Franci Stampar 1 1 University of Ljubljana, Biotechnical Faculty, Agronomy Department, Chair for Fruit Growing, Jamnikarjeva 101, SI-1000 Ljubljana, Slovenia 2 University of Graz, Institute for Plant Sciences, Schubertstraße 51, A-8020 Graz, Austria Abstract: Eleven organically grown apple cultivars and 11 apple cultivars of integrated production from Austria and Slovenia were analyzed by HPLC for the content of phenolic compounds in peel and pulp. We identified chlorogenic acid, p-coumaric acid, procyanidin B3, protocatechuic acid, ( )-epicatechin, phloridzin, rutin and quercetin-3-rhamnoside in apple peel. In apple pulp, (+)-catechin was also identified in all the cultivars. Some other phenols (procyanidin B3, rutin and quercetin-3-rhamnoside) could not be identified or were not properly separated. With regard to the phenolic content in the apple peel, there were no differences between organically grown apple cultivars and apple cultivars of integrated production. Organically grown apples, however, exhibited a higher content of phenolic substances in the apple pulp compared with the apple cultivars of integrated production. This may be due either to the different genotype source or to the growing technology. Higher concentrations of phenolic compounds in organically grown cultivars could be a result of plant response to stress. The apple peel contained higher concentrations of identified phenols than the pulp. The apple peel represents up to 10% of the whole fruit; therefore the phenolsic compounds in the pulp are of greater importance to the consumer than the phenolic compounds in the peel Society of Chemical Industry Keywords: apple; phenolic compounds; peel; pulp; integrated fruit production; organic fruit production INTRODUCTION Apples, like other fruits, vary in chemical composition, even within the same variety, depending on maturity, location of production, and agricultural practices, as well as on numerous environmental factors. 1,2 However, every cultivar has its own typical chemical composition. Phenolic compounds are naturally occurring plant secondary metabolites which determine outer and inner quality parameters of fruits such as appearance, flavor and health-promoting properties. 3,4 These naturally occurring antioxidants have been reported to contribute against oxidative damage caused by free radicals. 1 Some of these compounds have even stronger antioxidant activity, for instance vitamin C. Lee et al 1 report that flavanoids such as quercetin, epicatechin and procyanidin B2, rather than vitamin C, contribute significantly to the total antioxidant activity of apples. Adding to this, phenolics in the apple peel show a much higher contribution to total antioxidant activity of the whole apple than apple pulp, 5 so it is highly desirable to consume apples with the peel in order to maximize the apple antioxidant activity. Lee et al 1 also argue that there is increasing evidence of flavanoids being absorbed into the human body in amounts that are sufficient to exert anitoxidant and other biological activities in vivo. Freeforms of flavonoids and isoflavones are supposed to have a higher biological activity compared with their derivates in vitro. In addition to antioxidant effects, polyphenolic compounds have beneficial influence against development of cancer and coronary heart diseases and they lower the risks of brain and immune dysfunction, stroke and other diseases. 3 Phenolics as bioactive compounds play an important role in the plant defense mechanism as well as in the antioxidant expression of the plant. It is known that the phenolic composition of a plant tissue can determine the level of susceptibility/tolerance to fungal infections and pests. 6,7 Some studies have been performed to evaluate the impact of cultural practice (organic vs conventional production) in different fruit species on the polyphenol content The authors reported Correspondence to: Robert Veberic, University of Ljubljana, Biotechnical Faculty, Agronomy Department, Chair for Fruit Growing, Jamnikarjeva 101, SI-1000 Ljubljana, Slovenia robert.veberic@bf.uni-lj.si (Received 31 May 2003; revised version received 1 September 2004; accepted 20 October 2004) Published online 31 March Society of Chemical Industry. J Sci Food Agric /2005/$
2 R Veberic et al mainly an increase in the total phenolic content in the fruit trees grown organically. On the other hand, Lombardi-Boccia et al 10 reported higher total polyphenol contents in conventional plums. It is also a general opinion that organically grown fruit from old varieties should be healthier compared with the fruits of modern cultivars from intensive orchards. Therefore the aim of our study was to scan the phenolic composition of the apple pulp and peel of different cultivars, which were grown either organically or in integrated production. Organically grown apples, as well as resistant cultivars, exhibit higher natural resistance to pest and diseases, so we hypothesized that the fruits of those cultivars have higher contents of phenolic compounds in the peel and pulp compared with the apples from integrated production. Owing to biotic and abiotic stressors, we assumed that the content of phenolic compounds would be higher in the peel than in the pulp. MATERIAL AND METHODS Plant material The cultivars were obtained from the apple orchards in Styria (Austria) and Štajerska (Slovenia). The same cultivars are widespread in both countries because of their common history. The technology of fruit production in these orchards was either organic (O) or integrated (I). We also included three scab-resistant cultivars (R). Organic production means that, in the production of those fruit trees, no synthetic chemicals are used, but only natural substances. Integrated production (also called environmentally friendly production) includes the use of chemicals according to precise guidelines and restrictions for their use, especially in the protection of the plants against pests and diseases. Resistant cultivars were cultivated as the integrated ones, but they were not sprayed against apple scab caused by the fungus Venturia inaequalis, to which they are supposed to be resistant or tolerant. The organically grown cultivars (German/Slovenian names) were: Großer rheinischer Bohnapfel / Bobovec, Kronprinz Rudolf / Carjevič, Gravensteiner / Grafenštajnc, Rheinischer Krummstiel / Krivopecelj, Kornapfel, Steirischer Maschanzker / Štarjerski mošancelj, Geflammter Kardinal / Pisani Kardinal, Železničarka, Goldparmäne / Zlata Parmena, Roter Pogatscher / Štajerski Pogačar and Champagner Renette / Šampanjska Reneta. The cultivars of integrated production were: Royal Gala, Fuji, Elstar, Jonagold Decosta, Jonatan, Majda, Pink Lady and Braeburn. The resistant cultivars were Pinova, Remura and Topaz. The fruits were harvested at optimal ripening time. Phenolic compounds were analyzed in the pulp and peel of the apples. For every cultivar three replications were done (n = 3), each repetition including 15 apples sampled from five trees. The peel was separated from the pulp and both were stored at 20 C until preparation of the samples. Chemicals For the determination of obtained peaks we used standards acquired from Fluka [( )-epicatechin, p- coumaric acid, quercetin-3-rhamnoside and phloridzin], Sigma (rutin, procyanidin B3 and chlorogenic acid), Merck (protocatechuic acid) and Roth [(+)- catechin]. Methanol for liquid chromatography was acquired from Merck. Water was bi-distilated using Milli-Q system (Millipore). Extraction and HPLC analysis The samples were prepared according to the method described by Escarpa and Gonzalez. 11 The samples of 10 and 5 g of pulp and peel were extracted with methanol containing 1% 2,6-di-tert-butyl-4- methylphenol (BHT) using an ultrasonic bath. The samples were extracted with 10 ml of solvent for 1 h, 10 ml for 30 min, and finally 5 ml for 30 min. The tree extraction fractions were combined to a final volume of 25 ml and filtered through 0.25 µm membrane filter (Mecherey-Nagel) prior to the injection on to the HPLC system. BHT was added to samples to prevent their oxidation during the extraction. It did not interfere with the extracted phenols or during the subsequent HPLC analysis, because it was eluted at the end of the gradient or in the equilibration delay between the two analyses. The samples were analyzed on Thermo Finnigan Surveyor HPLC system with diode array detector at 280 nm. The spectra of compounds were also recorded between 210 and 350 nm. The elution solvents were aqueous 0.01 M phosphoric acid (A) and 100% methanol (B). The samples were eluted according to a linear gradient described by Escarpa and Gonzalez 11 with minor modifications: 5 50% B (10 min), 50 70% B (5 min), 70 80% B (5 min) and finally % B (for 5 min). The injection amount was 20 µl and the flow rate was 1 ml min 1. The column used was a Varian Hypersil 5 ODS HPLC column, operated at 25 C. Identification of compounds was achieved by comparing the retention times and spectra as well as with addition of the internal standard. The concentrations of phenolic compounds were calculated with the help of a corresponding external standard. The concentrations were expressed as mg 100 g 1 fresh weight (FW). Statistical analysis The significance of the type of cultivation and the content of phenolics in the peel and pulp of individual varieties were analyzed with the program Statgraphics plus 4.0 using analysis of variance (ANOVA). The differences between the treatments were estimated with a multiple range test using the least significant difference (LSD) or Duncan test at α< J Sci Food Agric 85: (2005)
3 Phenolic compounds in some apple cultivars RESULTS AND DISCUSSION Content of phenolic compounds in the apple peel In the study, we identified chlorogenic acid, p- coumaric acid (hydroxycinnamic acids), procyanidin B3 (procyanidins), protocatechuic acid (benzoic acids), ( )-epicatechin (catechins), phloridzin (dihydrochalcones), rutin and quercetin-3-rhamnoside (flavonols) in the apple peel (Fig 1). Data are shown in Table 1. Some other phenolic compounds were also identified [caffeic acid, syringic acid, (+)-catechin], but the data are not shown due to some difficulties with proper integration as a consequence of nonoptimal separation of these compounds. Also, the values of rutin (quercetin-3-rutinoside) are quite high compared with the results achieved by other authors, who report values in the range of mg 100 g 1 FW 12. Such values were present in our study only from a few cultivars with the lowest content of rutin. Our results agree more with those by Escarpa and Gonzalez, 11 whose method we used for the extraction and analysis. They determined the amounts of rutin in the apple peel up to 67 mg 100 g 1 FW. According to analyzed spectra, we assume that the peak of rutin could also include other quercetin glycosides. With the exception of rutin, the most pronounced phenols were chlorogenic acid, phloridzin and quercetin-3-rhamnoside. Other authors 13,14 reported high amounts of chlorogenic acid and phloridzin as well. Tsao et al 15 reported that the amount of chlorogenic acid in the peel in eight different apple cultivars was on average 13.6 mg 100 g 1 FW. The average chlorogenic acid content in our 22 cultivars was 27.0 mg 100 g 1. The highest value was achieved at the organically grown cultivar Bohnapfel, namely 79.5 mg 100 g 1. Organically grown cultivars, when compared as a group, showed higher amounts of chlorogenic acid than the cultivars of integrated production, and resistant cultivars. The same held true for most of the other phenolic compounds found in the apple peel. Chlorogenic acid also had an important antioxidative capacity, comparable to ascorbic acid (vitamin C). 1 The phloridzin content in our apples ranged from 5.0 to 25.2 mg 100 g 1 FW. That is in the range mg 100 g 1 FW reported by Perez- Ilzarbe et al. 12 Again the highest value was achieved by the organically grown cultivar Železničarka, but some intensively grown apples also achieved high values (ie Pink Lady ). Hock and Elstner 7 reported that leaves of apple trees, which are resistant against apple scab caused by Venturia inaequalis, contain a high content of phloridzin. In the pulp and peel of resistant apple cultivars phloridzin was found, but the content of phloridzin in the resistant cultivars Pinova, Remura and Topaz was similar to that measured in the cultivars of integrated production, and lower than in organically produced cultivars. A high content of quercetin-3-rhamnoside was also identified in some cultivars, ranging from 1.2 to 49.4 mg 100 g 1. The highest value was found in the intensively grown cultivar Jonagold Decosta. Other authors identified other quercetin glycosides as more important (ie galactoside, arabinoside). 15 Lee et al 1 reported that quercetin is an important phenol with antioxidative properties, however it is much more easily taken up in the human body in the form of glycosides, which are afterwards transformed into quercetin. Therefore the amount of quercetin glycosides could be important for nutritional value of apples. Procyanidins are also supposed to contribute to the antioxidative potential of apple fruit. 1 In our study procyanidin B3 was identified according to the external standard. Other authors report mainly procyanidin B1 and B2 to be found in the apple peel. 4,15 The range 1500 mau (-)-epicatechin phloridzin Q-3-rhamnozide mau procyanidin B3 protocatechuic acid chlorogenic acid p-coumaric acid rutin Minutes Figure 1. HPLC chromatogram of the apple peel of the cultivar Bohnapfel. J Sci Food Agric 85: (2005) 1689
4 R Veberic et al Table 1. Content of phenolic compounds in the apple peel (mg 100 g 1 FW) in different apple cultivars. Means and standard errors are presented. Cultivar TYP Procyanidin B3 Protocatechuic acid Chlorogenic acid ( )-Epicatechin p-coumaric acid Rutin Phloridzin Quercetin-3-rhamnozide Bohnapfel O 3.2 ± ± ± ± ± ± ± ± 6.5 Kronprinz O 1.8 ± ± ± ± ± ± ± ± 2.1 Gravensteiner O 5.1 ± ± ± ± ± ± ± ± 9.9 Krummstiel O 1.7 ± ± ± ± ± ± ± ± 2.7 Kornapfel O 1.8 ± ± ± ± ± ± ± ± 0.7 St Maschanzker O 2.4 ± ± ± ± ± ± ± ± 1.7 Geflammter Cardinal O 2.1 ± ± ± ± ± ± ± ± 0.8 Železničarka O 3.2 ± ± ± ± ± ± ± ± 1.1 Goldparmäne O 2.5 ± ± ± ± ± ± ± ± 0.2 Roter Pogatscher O 5.7 ± ± ± ± ± ± ± ± 3.0 Champagner Renette O 2.8 ± ± ± ± ± ± ± ± 2.9 Royal Gala I 3.5 ± ± ± ± ± ± ± ± 1.7 Fuji I 0.6 ± ± ± ± ± ± ± ± 10.8 Elstar I 3.5 ± ± ± ± ± ± ± ± 2.0 Jonagold Decosta I 2.0 ± ± ± ± ± ± ± ± 13.5 Jonatan I 3.7 ± ± ± ± ± ± ± ± 1.0 Majda I 1.6 ± ± ± ± ± ± ± ± 2.5 Pink Lady I 1.5 ± ± ± ± ± ± ± ± 1.4 Braeburn I 1.8 ± ± ± ± ± ± ± ± 3.3 Pinova R 2.6 ± ± ± ± ± ± ± ± 1.3 Remura R 2.2 ± ± ± ± ± ± ± ± 0.2 Topaz R 1.9 ± ± ± ± ± ± ± ± 3.6 O b b a ab b α = 0.05 I NS a a b NS b ab NS R b a ab a a TYP = type of production; O = cultivars of organic fruit production; I = cultivars of integrated fruit production; R = scab-resistant cultivars; n = 3. (a, b) Different letters indicate significant differences between treatments. NS = non-significant differences between treatments. The differences between treatments are significant at α<0.05 (5% degree of risk) J Sci Food Agric 85: (2005)
5 Phenolic compounds in some apple cultivars of procyanidin B3 found in the fruits was between 0.6 mg 100 g 1 in the cultivar Fuji and 5.7 mg 100 g 1 in the organically grown cultivar Štajerski pogačar. This was also in the range of protocatechuic acid (0.3 3 mg 100 g 1 FW) and epicatechin ( mg 100 g 1 FW). The content of p-coumaric acid was even lower (average value 0.4 mg 100 g 1 FW). Considering all analyzed phenolic compounds, we can see that the organically grown cultivar Bohnapfel had the highest content of total phenolics. Of the intensively grown cultivars, Pink Lady had the highest content of total phenolics analyzed in the study. There were no significant differences in the total phenolics in the peel between organically grown cultivars, intensively grown cultivars and scab resistant cultivars. Content of phenolic compounds in the apple pulp Owing to a better separation from the apple pulp (+)- catechin was also identified in all cultivars, while some other phenols (procyanidin B3, rutin and quercetin- 3-rhamnoside) could not be identified or properly separated in all cultivars (Fig 2, Table 2). In general, there was a lower content of individual phenolics in the fruit pulp, compared with the phenolics in the apple peel. The relationship between the content of individual phenolics in the apple peel and apple pulp is presented in Table 3. Chlorogenic acid was present at the highest concentration in the apple pulp, ranging from 1.0 in the cultivar Majda to 39.6 mg 100 g 1 FW in the cultivar Bohnapfel. Tsao et al 15 achieved similar results in eight apple cultivars, with a mean value of 17.7 mg 100 g 1 for chlorogenic acid. In their study, chlorogenic acid was also the most prominent phenolic found in the apple pulp. The contents of chlorogenic acid in the peel and pulp were quite similar. This was not the case with other investigated phenols whose contents in the peel and pulp exhibited greater differences. In organically grown cultivars, the concentration of chlorogenic acid in the peel was from 0.68 to 2.18 times higher than in the pulp (Table 3). This was quite a low range compared with the apples from integrated production, where the range was from 1.23 to 5.50, and resistant cultivars, with a ratio from 1.85 to The results achieved by Galvis Sanchez et al 16 also showed that the amount of chlorogenic acid in pear peel was higher than in the pulp. The second highest amounts of determined phenols in the pulp were those of (+)-catechin with an average value of 0.85 mg 100 g 1 FW of pulp. This was slightly lower than the amount reported by Escarpa and Gonzalez, 11 who noted values of (+)-catechin ranging from 0.28 to 18.2 in the pulp of Granny Smith apples. The highest value of (+)-catechin in our study was achieved with Elstar, namely 3.5 mg 100 g 1 FW. Similar values to (+)-catechin were found for phloridzin with mean value of 0.75 mg 100 g 1 FW. Those values were also obtained in the analysis by Tsao et al. 15 The content of phloridzin differed markedly between the peel and pulp content. In some cultivars, the content of phloridzin was from 60 to 100-fold lower in the pulp than in the peel (Table 3). The average values for the contents of protocatechuic acid, ( )-epicatechin and p-coumaric acid were 0.24, 0.51 and 0.16 mg 100 g 1 FW, respectively. For all three phenolic compounds, the relationship of the content in the peel and pulp was tighter in organically grown apples than in intensively grown ones (Table 3). Organically grown cultivars showed significantly higher contents of total phenolic compounds analyzed in the apple pulp compared with the apples of (-)-epicatechin 300 mau mau protocatechuic acid (+)-catechin chlorogenic acid p-coumaric acid phloridzin Minutes Figure 2. HPLC chromatogram of the apple pulp of the cultivar Bohnapfel. J Sci Food Agric 85: (2005) 1691
6 R Veberic et al Table 2. Content of phenolic compounds in the apple pulp (mg 100 g 1 FW) in different apple cultivars. Means and standard errors are presented. Cultivar TYP Protocatechuic acid (+)-Catechin Chlorogenic acid ( )-Epicatechin p-coumaric acid Phloridzin Bohnapfel O 0.31 ± ± ± ± ± ± 0.02 Kronprinz O 0.32 ± ± ± ± ± ± 0.03 Gravensteiner O 0.72 ± ± ± ± ± ± 0.20 Krummstiel O 0.19 ± ± ± ± ± ± 0.20 Kornapfel O 0.20 ± ± ± ± ± ± 0.14 St Maschanzker O 0.47 ± ± ± ± ± ± 0.18 Geflammter Cardinal O 0.32 ± ± ± ± ± ± 0.01 Železničarka O 0.25 ± ± ± ± ± ± 0.02 Goldparmäne O 0.11 ± ± ± ± ± ± 0.02 Roter Pogatscher O 0.73 ± ± ± ± ± ± 0.15 Champagner Renette O 0.22 ± ± ± ± ± ± 0.13 Royal Gala I 0.16 ± ± ± ± ± ± 0.01 Fuji I 0.08 ± ND 10.7 ± ± ± ± 0.15 Elstar I 0.23 ± ± ± ± ± ± 0.06 Jonagold Decosta I 0.14 ± ± ± ± ± ± 0.05 Jonatan I 0.12 ± ± ± ± ± ± 0.02 Majda I 0.06 ± ND 1.0 ± ± ± ± 0.03 Pink Lady I 0.07 ± ± ± ± ± ± 0.01 Braeburn I 0.12 ± ± ± ± ± ± 0.04 Pinova R 0.11 ± ± ± ± ± ± 0.01 Remura R 0.13 ± ± ± ± ± ± 0.06 Topaz R 0.12 ± ± ± ± ± ± 0.01 O b b b b b α = 0.05 I a NS a a a a R a a a a a TYP = type of production; O = cultivars of organic fruit production; I = cultivars of integrated fruit production; R = scab-resistant cultivars; n = 3. (a, b) Different letters indicate significant differences between treatments. NS = non-significant differences between treatments. The differences in treatments are significant at α<0.05 (5% degree of risk). Table 3. Relationship between the content of phenolic compounds in the apple peel and apple pulp (concentration in apple peel/concentration apple pulp) in different apple cultivars Cultivar TYP Chlorogenic acid Protocatechuic acid ( )-Epicatechin p-coumaric acid Phloridzin Bohnapfel O Kronprinz O Gravensteiner O Krummstiel O Kornapfel O St Maschanzker O Geflammter Cardinal O Železničarka O Goldparmäne O Roter Pogatscher O Champagner Renette O Royal Gala I Fuji I Elstar I Jonagold Decosta I Jonatan I Majda I Pink Lady I Braeburn I Pinova R Remura R Topaz R TYP = type of production; O = cultivars of organic fruit production; I = cultivars of integrated fruit production; R = scab-resistant cultivars J Sci Food Agric 85: (2005)
7 Phenolic compounds in some apple cultivars Table 4. Total phenols analyzed in the peel and pulp of different cultivars (mg g 1 FW) Cultivar TYP Peel Pulp Bohnapfel O Kronprinz O Gravensteiner O Krummstiel O Kornapfel O Steirischer Maschanzker O Geflammter Cardinal O Železničarka O Goldparmäne O Roter Pogatscher O Champagner Renette O Royal Gala I Fuji I Elstar I Jonagold Decosta I Jonatan I Majda I Pink Lady I Braeburn I Pinova R Remura R Topaz R O b α = 0.05 I NS a R a TYP = type of production; O = cultivars of organic fruit production; I = cultivarsofintegrated fruitproduction; R = scab-resistant cultivars; n = 3. (a, b) Different letters indicate significant differences between treatments. NS = non-significant differences between treatments. The differences between treatments are significant at α<0.05 (5% degree of risk). integrated production and resistant cultivars. There were no significant differences between resistant and intensively grown cultivars. The highest content of total phenolic compounds was in the cultivar Bohnapfel and the lowest content of total phenolics was measured in the cultivars Majda and Remura (Table 4). This is not only the consequence of the fact that organically grown apples are more exposed to biotic and abiotic stressors (diseases, pests, lack of mineral nutrients, etc), but also due to the selection of modern cultivars towards less tough fruits with a less astringent taste. The consumers prefer fruits with a milder taste 3, which leads to then choosing those modern cultivars that exhibit lower contents of some groups of phenolics. CONCLUSIONS The results achieved in the investigation of phenolic composition are comparable with the results achieved by other authors. With regard to the content of total phenolics analyzed in the apple peel, we did not notice differences between organically grown apple cultivars and the cultivars of integrated production. Genotype is probably one of the factors that markedly determine the content of individual phenolics. Organically grown apples, however, showed higher contents of phenolic substances in the apple pulp compared with apple cultivars of integrated production. This may be due either to the different genotype source or the type of growing technology. In the organic production, synthetic chemicals (fertilizers, pesticides as, thinners) that are used in integrated fruit production are not allowed. Therefore organically grown plants are exposed to different kinds of stress. More phenolic compounds in organically grown cultivars could be a mechanism of plant response to stress. The apple peel contained higher concentrations of phenols than the pulp; however, the peel represents, at a maximum, 10% of the whole fruit (depending on the fruit size and thickness of the peel). Therefore the phenols in the pulp are of greater importance to the consumer than the phenols in the peel. Because of lower contents of phenolics in the apples from integrated growth, the apple peel of those apples should not be removed before eating. REFERENCES 1 Lee KW, Kim YJ, Kim D, Lee HJ and Lee CY, Major phenolics in apple and their contribution to the total antioxidant capacity. J Agric Food Chem 51: (2003). 2 Šturm K, Hudina M, Solar A, Viršček-Marn M and Štampar F, Fruit quality of different Gala clones. Gartenbauwissenschaft 68: (2003). 3 Lattanzio V, Bioactive polyphenols: their role in quality and storability of fruit and vegetables. J Appl Bot 77: (2003). 4 Treutter D, Biosynthesis of phenolic compounds and its regulation in apple. Plant Growth Regul 34:71 89 (2001). 5 Eberhardt MV, Lee CY and Liu RH, Nutrition antioxidant activity of fresh apples. Nature 405: (2000). 6 Usenik V, Mikulič-Petkovšek M, Solar A and Štampar F, Flavonols of leaves in relation to apple scab resistance. 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