Variation of bioactive compounds content of 14 oriental strawberry cultivars

Food Chemistry 184 (2015) 196–202

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Variation of bioactive compounds content of 14 oriental strawberry cultivars Sung Kyeom Kim a,b, Dong Sub Kim c, Dae Young Kim b, Changhoo Chun a,c,⇑ a

Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Republic of Korea Vegetable Research Division, National Institute of Horticultural & Herbal Science, Wanju 565-852, Republic of Korea c Department of Plant Science, Seoul National University, Seoul 151-921, Republic of Korea b

a r t i c l e

i n f o

Article history: Received 25 November 2014 Received in revised form 14 March 2015 Accepted 18 March 2015 Available online 24 March 2015 Keywords: Anthocyanin Ascorbic acid Breeding program Ellagic acid Fragaria  ananassa

a b s t r a c t Variation in bioactive compounds content was assessed in antioxidant rich June-bearing strawberry cultivars. Ascorbic acid, anthocyanin, and ellagic acid content were analyzed in ripe fruits of 14 cultivars. The bioactive content in strawberry fruit was found to vary significantly among cultivars and from year to year. The highest ascorbic acid content was found in ‘Sugyeong’. The ‘Red Pearl’ and ‘Sachinoka’ had three to fourfold higher amounts of pelargonidin 3-glucoside than other cultivars. For cyanidin 3-glucoide and pelargonidin 3-rutinoside, two other characterized anthocyanins, ‘Dahong’ and ‘Keumhyang’ had the highest contents among all the tested cultivars. The ellagic acid content of ‘Dahong’ was generally all within the upper ranges. These results can be used for the validation of fruit antioxidant capacity and in addition, provide useful information for breeding programs looking to enhance the antioxidant capacity in strawberry fruit. Ó 2015 Elsevier Ltd. All rights reserved.

1. Introduction Strawberry (Fragaria  ananassa Dutch.) is one of the most commonly consumed small fruits, being utilized both in fresh and processed forms in jam, juice, yogurt, and even in dietary supplements. The significant economic and commercial impacts of strawberries have led to them being among the most heavily researched from the agronomic, genomic, and nutritional point of view. The nutritional quality of strawberry fruits has been correlated to the high content of bioactive compounds such as ascorbic acid (Giné Bordonaba & Terry, 2011), anthocyanin (Hannum, 2004), and ellagic acid (Mass, Galleta, & Stoner, 1991), most of which express relevant antioxidant capacities in vitro and in vivo (Olsson et al., 2004). Increasing evidence has highlighted that consuming strawberry fruits is beneficial for maintaining good health and reducing the risk of certain chronic diseases such as cancers (Seeram et al., 2006), cardiovascular disease (Azzini et al., 2010), and memory loss (Giampieri et al., 2012). Several studies have also suggested that polyphenols in strawberry fruits play a primary role in preventing cell damage due to the exposure to reactive oxygen species (Olsson et al., 2004; Rekika et al., 2005; Wang & Lewers, 2007). Given these important findings, consumers, growers, breeders, and processors have become more interested in health-beneficial compounds in strawberry fruits for their nutraceutical properties. ⇑ Corresponding author at: Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Republic of Korea. Tel.: +82 2 880 4567. E-mail address: [email protected] (C. Chun). http://dx.doi.org/10.1016/j.foodchem.2015.03.060 0308-8146/Ó 2015 Elsevier Ltd. All rights reserved.

The breeding programs for rich-nutritious and better-tasting cultivars might be successful if the variability and diversity of the bioactive compounds (Mezzetti, 2013). Diamanti et al. (2012, 2014), revealed that increasing nutritional quality and healthbeneficial compounds of strawberry fruits using wild and cultivated germplasm. Furthermore, the valuable for breeding programs have considered regarding flavor, studies of biochemical pathways and signaling compounds as well as marker development (Ulrich & Olbricht, 2014). In the present study, contents of ascorbic acid, individual anthocyanins such as pelargonidin 3-glucoside, cyanidin 3-glucoside, and pelargonidin 3-rutinoside, and ellagic acid were assessed in 14 oriental June-bearing strawberry cultivars recently bred in Korea and Japan. In addition, in this investigation the bioactive compounds content were compared, in order to individuate compound for strawberry discrimination and individuation of strawberry cultivars with high content of those secondary metabolites. Thus, these results will be providing useful information for selective strawberry breeding. 2. Materials and methods 2.1. Strawberry samples Fruit samples were analyzed from 14 strawberry genotypes. These were: ‘Dahong’, ‘Keumhyang’, ‘Maehynag’, ‘Seolhyang’, ‘Ssanta’, ‘Sugyeong’, ‘Sunhong’ (Korean cultivars), and ‘Akihime’,

S.K. Kim et al. / Food Chemistry 184 (2015) 196–202

‘Benihoppe’, ‘Red Pearl’, ‘Sachinoka’, ‘Sagahonoka’, ‘Tochinomine’, and ‘Tochiotome’ (Japanese cultivars) (Table 1). Samples were collected from an experimental field established in the National Institute of Horticultural & Herbal Science experimental farm, located at Suwon, Korea (36° 430 N, 128° 070 E, and elevation 30 m). The experimental design was completely randomized with three replications. The cultivation type was substrate culture using drip irrigation system in a greenhouse. Strawberry plants (crown diameter: approximately 10 mm) were transplanted into plastic containers (740 mm  250 mm  200 mm, L  W  H) filled with a mixture of peatmoss (BM-4, Berger Peat Moss Ltd., Quebec, Canada) and perlite (Parat No 3, Kyung Dong Ceratech Co., Ltd., Seoul, Korea) (1:1, v/v). The plant density was 24 plants/m2. Mean daily average air temperature and integral radiation from flowering to harvest for fruit production years 2011 and 2012 were 0.6 and 0.7 °C, and 303.9 and 286.9 MJ m2, respectively. The night temperature inside the greenhouse was maintained above 10 °C. The secondary or tertiary strawberry fruits in the first cluster were harvested at the optimal fruit maturity when ca. 90% of the fruit surface had reached full red color. 2.2. Extraction and analysis of ascorbic acid Strawberry fruit sample (10 g) was homogenized with 50 mL of buffer solution (4% metaphosphoric acid) and filtered using an 8 lm cellulose filter paper (Whatman International Ltd., Kent, UK). The mixture was filtered through a 0.45 lm polyvinylidene fluoride membrane syringe filter (Agilent Co., Palo Alto, CA, USA) and injected into an HPLC system (Ultimate 3000, Dionex, Sunnyvale, CA, USA) under the following conditions. The mobile phase was acetonitrile and 50 mM NH4H2PO4 (70:30, v/v), and the flow rate was 1.0 mL/ min. The ascorbic acid components were detected at 254 nm. A C18 reverse phase column (4.6  250 mm, 0.5 lm; Supelcosil TM C-18, Supelco, Bellefonte, PA, USA) was used for analysis (Kim, Kim, & Park, 2006). Each measurement had three replications, three separate extractions from three different fruit samples.

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(Whatman International Ltd., Kent, UK), and then the solutions were filtered through a 0.45 lm polyvinylidene fluoride membrane syringe filter (Agilent Co., Palo Alto, CA, USA) prior to injection into an HPLC system (Ultimate 3000, Dionex, Sunnyvale, CA, USA). Solvents used were: (A) 0.1% trifluoroacetic acid in water, and (B) HPLC-grade acetonitrile, establishing the following gradient: isocratic 10% of B for 5 min, 10–15% of B over 15 min, isocratic 15% of B for 5 min, 15–18% of B over 5 min, and 18–35% of B over 20 min, using a flow rate of 0.5 mL min1. Separation was achieved using a C18 column (4.6  150 mm, 5 lm; Zorbax SB-C18, Agilent Co., New York, USA) and peaks were identified with a UV/Vis detector at 520 nm (da Silva, Escribano-Bailon, Alonso, Rivas-Gonzalo, & Santos-Buelga, 2007). Individual anthocyanin standards (Pelargonidin 3-glucoside, pelargonidin 3-rutioside, and cyaniding 3-glucoside) were purchase from Extrasynthese SA. (Lyon, Nord Genay, France). Each measurement had three replications, three separate extractions from three different fruit samples. 2.4. Extraction and analysis of ellagic acid Strawberry fruit samples (2.5 g) were homogenized in 7.5 mL of purified water, and 12.5 mL of methanol was added. In addition, 5.0 mL of 6.0 mol L1 HCl was added. The mixtures were refluxed for 2 h at 85 °C and then filtered through a 0.45 lm polyvinylidene fluoride membrane syringe filter (Agilent Co., Palo Alto, CA, USA) prior to injection into an HPLC system (Ultimate 3000, Dionex, Sunnyvale, CA, USA). Solvent A was 1% formic acid and solvent B was acetonitrile with 0.5 mL/min flow rate. The gradient was: 0–15 min, 10–55% of B in A; 15–20 min, 55–100% of B in A; 20– 25 min, 100–10% of B in A; 25–35 min, 10–10% of B in A. Separation was achieved using a C18 column (4.6  150 mm, 5 lm; Zorbax SB-C18, Agilent Co., Palo Alto, CA, USA) and peaks were identified using UV/Vis detector at 260 nm (Kim, Bea, Na, Ko, & Chun, 2013). Each measurement had three replications, three separate extractions from three different fruit samples. 2.5. Statistical analysis

2.3. Extraction and analysis of anthocyanin Anthocyanin was extracted from the fruit skin (2 g), less than 2 mm thick, by homogenizing with 5 mL HCl (1%)-methanol solution. The extract was filtered through an 8 lm cellulose filter paper

Influence of strawberry cultivars and years on health-related compounds in strawberry fruit was assessed using Analysis of Variance (ANOVA) in SAS 9.2 (SAS Institute Inc., Cary, NC, USA) to identify least significant differences (P < 0.001).

Table 1 Parentage and origin of 14 June-bearing strawberry cultivars.

3. Results and discussion

Cultivar

Parentage

Origina

Dahong Keumhyang Maehyang Seolhyang Ssanta Sugyeong Sunhong Akihime

Sachinoka  Maehyang Akihime  Red Pearl Tochinomine  Akihime Akihime  Red Pearl Maehyang  Seolhyang Johong  Maehyang Johong  Maehyang Kunowase  Nyoho

Benihoppe Red Pearl

Akihime  Sachinoka Aiberry  Toyonoka

Sachinoka Sagahonoka Tochinomine

Toyonoka  Aiberry Oonish  Toyonoka (Florida 69– 226  Reiko)  Nyoho Kurume 49  Tochinomine

NIHHS, South Korea, 2007 NSES, South Korea, 2005 NSES, South Korea, 2001 NSES, South Korea, 2005 SFVES, South Korea, 2009 NIHHS, South Korea, 2008 NIHHS, South Korea, 2005 Ogiwara, A. in Shizuoka, Japan, 1992 SAES, Japan, 2002 Nishida, A. in Ahime, Japan, 1993 KBNRIVOT, Japan, 1996 SGAES, Japan, 2001 TAES, Japan, 1993

Tochiotome a

TAES, Japan, 2006

NIHHS, National Institute of Horticultural & Herbal Science, RDA, South Korea; NSES, Nonsan Strawberry Experiment Station, South Korea; SFVES, Seongju Fruit Vegetable Experiment Station, South Korea; SAES, Shizuoka Agricultural Experiment Station, Japan; KBNRIVOT, Krume Branch of National Research Institute Vegetable, Ornamental, and Tea, Japan; SGAES, Saga Agricultural Experiment Station, Japan; TAES, Tochigi Agricultural Experiment Station, Japan.

3.1. Ascorbic acid content Ascorbic acid content strongly differed among cultivars and fruit production years (Table 2). Across fruit production year, ascorbic acid content ranged from 56.8 to 108.1 mg/100 g fresh weight (Fig. 1). The highest ascorbic acid content was found for ‘Sugyeong’ harvested in 2011, while low content was analyzed for ‘Sagahonoka’ and ‘Seolhyang’ harvested in 2012. The ‘Sugyeong’ showed higher contents of dietary antioxidant such as ascorbic acid. This ‘Sugyeong’ could thus be useful for developing cultivars with high antioxidant capacity. Significant variation in different quality traits and antioxidants by strawberry cultivars were also reported by Capocasa, Scalzo, Mezzetti, and Battino (2008), Singh et al. (2011), Tsao et al. (2005) and Wang and Jiao (2000). The ascorbic acid content of ‘Sagahonoka’ and ‘Seolhyang’ harvested in 2011 was 23.7% and 34.4% lower than that of fruits harvested in 2012. Ascorbic acid content of ‘Sagahonoka’ and ‘Seolhyang’ was most easily influenced by changes in environmental conditions. Ascorbic acid content can be modified by several pre-harvest factors (Lee & Kader, 2000). Among them, light

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Table 2 Analysis of variance for health-related compounds of selected strawberry cultivars.

z,⁄

Variable

d.f.

Year (A) Cultivar (B) AB

1 13 13

or

⁄⁄⁄

Ascorbic acid

Pelargonidin 3-glucoside

Cyanidin 3-glucoside

Pelargonidin 3rutinoside

Ellagic acid

Mean square

F value

Mean square

F value

Mean square

F value

Mean square

F value

Mean square

F value

740.5 715.9 191.3

14.7⁄⁄⁄z 14.2⁄⁄⁄ 3.8⁄⁄⁄

2690.8 825.5 83.6

162.2⁄⁄⁄ 49.8⁄⁄⁄ 5.0⁄⁄⁄

16.0 8.0 2.2

34.2⁄⁄⁄ 17.2⁄⁄⁄ 4.6⁄⁄⁄

0.3 1.7 0.1

12.5⁄⁄⁄ 67.6⁄⁄⁄ 2.2⁄

171.1 17.1 16.7

134.8⁄⁄⁄ 13.5⁄⁄⁄ 13.2⁄⁄⁄

Significant at P 6 0.05 or 0.001, respectively.

2011 2012

Ascorbic acid content (mg/100 g fresh weight)

120

100

80

60

40

20

0 Da

ho

ng Ke

hy um

an

e a e e a e g g g ta ng arl in pp an ok ok im on on an om ya Pe in ih hy ho on ye om hiot nh Ss i h lh k d h g n u c n o e i ae A S c ga R Su Sa ch M Se Be To Sa To Korean cultivars Japanese cultivars

g

Fig. 1. Comparison of ascorbic acid content in 14 different June-bearing strawberry cultivars harvested from two different fruit production years.

intensity increases sugar production and, as a consequence, may increase ascorbic acid synthesis. In contrast, temperature has been suggested to have an inverse effect (Wang & Camp, 2000); with higher day and night temperatures leading to decreased synthesis of sugar and ascorbic acid (Kim et al., 2013). In addition, fruit quality were influenced by latitude and thus temperature giving northern sites in general the highest values of dry matter, soluble solids and titratable acidity (Krüger et al., 2012). 3.2. Pelargonidin 3-glucoside content The mean square showed that the contents of pelargonidin 3-glucoside (Pg), major anthocyanin of strawberry varied significantly among the genotypes and between fruit production years (Table 2). The Pg ranged from 15.6 to 59.3 mg 100 g1 FW and 8.4 to 39.4 mg/100 g fresh weight for 2011 and 2012 fruit production years, respectively (Fig. 2a). The ‘Red Pearl’ and ‘Sachinoka’ had significantly higher content of Pg content compared with all other fruits, having three to fourfold more. Variation in Pg content between the two fruit production years was also observed. This is in accordance with previous reports of variation in anthocyanin concentration for a cultivar from year to year (da Silva et al., 2007; Wang, Zheng, & Galleta, 2002). The strawberry variety ‘Elsanta’, grown in the same conditions and harvested at the same ripening stage and at the same date, during two consecutive production years showed some differences in their content in phenolics (Pincemail, Kevers, Tabart, Defraigne, & Dommes, 2012). The Pg content of all the cultivars was higher for the 2011 fruit production year than in 2012 except in the case of ‘Tochinomine’ showing similar Pg content both in 2011 and 2012. It is thus likely that the various cultivars are probably differently affected by variations in growing conditions. Several studies have suggested that annual variation in phytochemical composition could be attributable to

variations in solar radiation and air temperature (Crespo, Giné Bordonaba, Terry, & Carlen, 2010; Olsson et al., 2004). In particular, anthocyanin content variation among different fruit production years may be related to yearly variation in solar radiation and air temperature (Kim et al., 2012; Wang, Zheng, & Galleta, 2002). 3.3. Cyanidin 3-glucoside content The mean square showed that cyanidin 3-glucoside (Cg) content significantly varied among the genotypes and between fruit production years (Table 2). Fig. 2b shows the Cg content in the assessed cultivars in two consecutive production years. Across fruit production year, the abundance of Cg differed by 15.5-fold among genotypes and ranged from 0.4 to 6.5 mg/100 g fresh weight with an average value of 2.0 mg/100 g fresh weight. Cg content was significantly higher in ‘Dahong’, followed by ‘Sunhong’, ‘Keumhyang’, ‘Tochinomine’, and ‘Sachinoka’ in 2011. However, in 2012, Cg content was significantly higher in ‘Tochinomine’ followed by ‘Dahong’, ‘Maehyang’, ‘Sunhong’, ‘Keumhyang’, with the lowest Cg content observed in ‘Sagahonoka’ and ‘Seolhyang’ in both years. 3.4. Pelargonidin 3-rutinoside (Pr) content The mean square showed that the contents of pelargonidin 3-rutinoside (Pr) varied significantly among the genotypes and between fruit production years (Table 2). Across fruit production years, the Pr contents ranged from 0.1 to 2.2 mg/100 g fresh weight (Fig. 2c). The highest Pr content was found for ‘Keumhyang’ harvested in both 2011 and 2012, while low content was analyzed for ‘Akihime’ and ‘Benihoppe’. Pr was not detected in ‘Dahong’, ‘Maehyang’, ‘Seolhyang’, ‘Santa’, and ‘Tochinomine’ from either year. The synthesis of Pr seems to be genetically controlled and previous works had demonstrated that, among 20 Japanese

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Pelargonidin 3-glucoside content

60

A

50 40 30 20 10 0

Cyanidin 3-glucoside content

B 8

6

4

2

0

Pelargonidin 3-rutinoside content

C

2011 2012

4

3

2

1 ND 0

ND

ND

ND

ND

e g g rl ta pe ne ka ka ng ng me an an ea an ya no no eo to him ihop mi ho ho hy hy Ss hi io ki dP ho gy no un c Da mh n ol e h i ae a u A S a e e c u g R S S ch M S B To Ke Sa To ng

ng

Korean cultivars

Japanese cultivars

Fig. 2. Comparison of individual anthocyanin contents such as pelargonidin 3-glucoside (A), cyaniding 3-glucoside (B), and pelargonidin 3-rutinoside (C) from 14 different June-bearing strawberry cultivars harvested from two different fruit production years. Y axis unit is mg/100 g fresh weight.

cultivars nine did not produce pelargonidin-3-malonylglucoside, while in the remaining 11 cultivars pelargonidin-3-malonylglucoside constituted 5–24% of total anthocyanins and the percentage was relatively constant throughout the coloring period (Yoshida, Koyama, & Tamura, 2002). Red color, which is a result of anthocyanin accumulation, usually occurs in the achenes, followed by the epidermis and finally in the inner receptacle tissue. Anthocyanin concentration in the cortex and pith was significantly lower in Korean and Japanese cultivars compared to European cultivars (Yoshida & Tamura, 2005). This difference may reflect cultural preferences, as in Korea and Japan strawberries are consumed intact and the color of the inner flesh may be less important than in Europe where the berries are frequently cut and displayed or processed. The Pr contents of ‘Keumhyang’, ‘Akihime’, ‘Red Pearl’, ‘Sachinoka’, and ‘Tochiotome’ harvested in 2012 were over 50% higher compared with that of fruits harvested in 2011 (Fig. 2c). When the day/night temperatures increased, fruit surface and flesh color became darker and redder, and antioxidant capacity significantly increased (Wang & Zheng, 2001). In addition, fruits

sampled at the southern sites (warm) were redder compared to those of the north (Krüger et al., 2012). 3.5. Sum of individual anthocyanin (SIA) content and ratio of Pg and Cg The mean square showed that sum of individual anthocyanin (SIA) contents and the ratio of Pg and Cg varied significantly among strawberry genotypes and between fruit production years (Table 3). The SIA contents ranged from 17.4 to 63.4 mg/100 g fresh weight and 9.2 to 42.5 mg/100 g fresh weight in 2011 and 2012, respectively. Total anthocyanins ranged between 21 and 49 mg/100 g fresh weight, with an average of 34 mg/100 g fresh weight, which is roughly similar to anthocyanin concentration previously reported in various strawberry cultivars (Aaby, Skrede, & Wrolstad, 2005; Buendia et al., 2010; da Silva et al., 2007; Määttä-Riihinen, KamalEldin, & Törrönen, 2004). We found significant differences among genotypes and production years, suggesting that both genetic and climatic factors have strong influence on the anthocyanin levels.

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Table 3 Effect of cultivar and fruit production year on the sum of individual anthocyanins and ratio of pelargonidin 3-glucoside and cyanidin 3-glucoside. Data is expressed as means ± SE. Cultivar

Fruit production year (2011)

Dahong Keumhyang Maehyang Seolhyang Ssanta Sugyeong Sunhong Akihime Benihoppe Red Pearl Sachinoka Sagahonoka Tochinomine Tochiotome

z,⁄⁄

Sum of individual anthocyanin (mg/ 100 g fresh weight)

Pelargonidin 3glucoside/cyanidin 3-glucoside

Sum of individual anthocyanin (mg/ 100 g fresh weight)

Pelargonidin 3glucoside/cyanidin 3-glucoside

48.1 ± 6.8 50.0 ± 7.0 20.5 ± 12.3 23.6 ± 3.1 30.8 ± 1.7 17.4 ± 3.6 28.2 ± 5.1 33.5 ± 4.9 20.9 ± 4.4 61.7 ± 7.5 63.4 ± 2.7 21.2 ± 1.7 36.6 ± 5.3 35.2 ± 5.6

6.7 ± 0.9 13.0 ± 1.6 13.2 ± 2.5 34.9 ± 1.6 28.4 ± 5.3 11.9 ± 0.9 6.6 ± 0.4 13.9 ± 1.1 8.8 ± 0.7 26.6 ± 3.0 16.9 ± 1.2 48.3 ± 2.2 9.6 ± 0.8 16.1 ± 0.3

30.5 ± 2.2 27.8 ± 3.6 18.0 ± 2.0 14.9 ± 0.5 20.7 ± 1.7 11.5 ± 0.6 18.7 ± 1.5 13.8 ± 0.6 9.2 ± 0.6 35.8 ± 1.3 42.5 ± 2.7 12.4 ± 0.5 38.5 ± 2.8 27.8 ± 1.5

10.0 ± 0.2 15.6 ± 2.0 8.3 ± 0.9 21.5 ± 3.8 16.0 ± 0.4 8.1 ± 1.1 9.9 ± 0.6 11.2 ± 1.0 13.9 ± 1.0 35.8 ± 7.8 21.4 ± 4.2 22.1 ± 3.5 8.7 ± 0.4 12.7 ± 0.8

Variable

d.f.

Year (A) Cultivar (B) AB

1 13 13

or

⁄⁄⁄

Fruit production year (2012)

Sum of individual anthocyanin

Pelargonidin 3-O-glucoside/cyanidin 3-Oglucoside

Mean square

F value

Mean square

F value

3059.2 952.4 97.4

140.4⁄⁄⁄z 43.7⁄⁄⁄ 4.5⁄⁄

171.7 486.2 129.9

9.2⁄⁄⁄ 26.2⁄⁄⁄ 7.0⁄⁄⁄

Significant at P 6 0.01 or 0.001, respectively.

2011 2012

Ellagic acid content (mg/100 g fresh weight)

20

15

10

5

0 Da

ho

e a e e e a g g g ta ng arl in an ok pp ok im on on an om ya Pe in ih hy ho on ye o m hiot nh Ss i h lh k d h g n u c n o e i ae A S c ga R Su Sa ch M Se Be To Sa To Korean cultivars Japanese cultivars

g

ng

an

Ke

hy um

Fig. 3. Comparison of ellagic acid content in 14 different June-bearing strawberry cultivars harvested from two different fruit production years.

The greatest SIA was found for ‘Sachinoka’ harvested in both fruit production years, while low content was analyzed for ‘Benihoppe’ and ‘Sugyeong’. We also found that certain cultivars (‘Sachinoka’, ‘Red Pearl’, ‘Dahong’, and ‘Keumhyang’) have potentially higher antioxidant values suggesting that breeding and selection could lead to new strawberry cultivars with greater antioxidant capacity. Various researchers indicated that the effect of genotype on strawberry antioxidant capacity and phenolic content is stronger than that of the environmental factors (Capocasa et al., 2008; Crespo et al., 2010). Across fruit production year, the ratio of Pg and Cg ranged from 6.7 to 48.3. The ‘Sagahonoka’, ‘Red Pearl’, and ‘Seolhyang’ had significantly higher ratios compared with all other fruits, having three- to eightfold more (Table 3). Previous works have shown that Pg was the most abundant anthocyanin in all the strawberry cultivars, contributing 60–95% to the total anthocyanin content,

followed by Cg (Aaby et al., 2005; Buendia et al., 2010; da Silva, Escribano-Bailon, Alonso, Rivas-Gonzalo, & Santos-Buelga, 2007; Määttä-Riihinen et al., 2004). Three major anthocyanins (Cg, Pg derivative and Pg at concentrations of 2.2, 33.6, and 121.5 mg/ 100 g1 fresh weight, respectively) were identified in strawberry genotype ‘Elsanta’ fruit grown in a glasshouse and subjected to full or deficit irrigation (Terry, Chope, & Bordonaba, 2007). Similar concentrations were later reported when studying anthocyanin concentrations in fruit from four different cultivars grown at different Swiss production sites (Crespo et al., 2010). In our study, the samples of all the tested cultivars had higher percentages of Pg (91%) and lower percentages of Cg (6%) and Pr (2%), while samples of genotype ‘Seolhyang’ possessed the highest proportions of Pg (96%) and the lowest ones of Cg (3%). The genotype ‘Red Pearl’ was the only variety that showed similar levels of Cg (3%) and Pr (3%).

S.K. Kim et al. / Food Chemistry 184 (2015) 196–202

3.6. Ellagic acid content The mean square showed that the contents of ellagic acid varied significantly among strawberry genotypes and between fruit production years (Table 2). Ellagic acid content in 14 different strawberry cultivars from both harvest years were presented in Fig. 3. The results showed great variation between production years and cultivars with values ranging from 1.1 to 15.0 mg/100 g fresh weight. The present results are in roughly the same range as those of previous researches (Atkinson et al., 2006; Mass, Galleta, & Stoner, 1991). They reported the ellagic acid concentrations ranging from 0.4 to 4.6 mg/100 g dry weight in different US-grown strawberry cultivars (roughly equivalent to 4.3–46.4 mg/100 g fresh weight) and from 6.0 to 34.1 in frozen weight in different UK-grown strawberry cultivars. Similarly, some results showed that ellagic acid concentrations in strawberries grown in Finland and Poland varied from 3.4 to 5.9 mg/100 g fresh weight (Häkkien, Kärenlampi, Mykkänen, Heinonen, & Törrönen, 2000). However, Williner, Pirovani, and Güemes (2003) measured lower ellagic acid concentrations of 0.2–0.5 mg/100 g fresh weight in Argentine-grown strawberries. The ellagic acid content in fruit grown during 2012 can be ranked in the following manner: ‘Dahong’ > ‘Keumhyang’ > ‘Red Pearl’ > ‘Sunhong’ > ‘Maehyang’ > ‘Tochiotome’ > ‘Sagahonoka’ > ‘Tochinomine’ > ‘Sugyeong’ > ‘Sachinoka’ > ‘Ssanta’ > ‘Seolhyang’ > ‘Akihime’ > ‘Benihoppe’. Total ellagic concentrations varied considerably over the two years. Interestingly, Korean cultivars such as ‘Dahong’, ‘Keumhyang’, ‘Maehyang’, and ‘Sunhong’ were generally all within the upper ranges, although the individual cultivar rankings differed between years. The ellagic acid can vary significantly from year to year and that of ‘Dahong’, ‘Keumhyang’, ‘Maehyang’, ‘Seolhyang’, ‘Sunhong’, ‘Akihime’, and ‘Red Pearl’ harvested in 2012 increased by over 50% compared with that in 2011. Comparison of year-to-year variation in total ellagic acid contents showed significant differences between cultivars such as ‘Symphony’, ‘Cambridge Favourite’, and ‘Elsanta’ (Atkinson et al., 2006). 4. Conclusion The research demonstrated that 14 selected Korean and Japanese strawberry cultivars had significant differences in ascorbic acid, anthocyanin, and ellagic acid contents over two harvest years. The ‘Sugyeong’, ‘Sachinoka’, ‘Red Pearl’, ‘Dahong’, ‘Keumhyang’, and ‘Maehyang’ were found to possess the highest content of health-related compounds. The information from this research could be useful in future breeding programs by identifying new cultivars with enhanced health-related compounds in strawberry fruits. Acknowledgments This work was carried out with the support of ‘‘Cooperative Research Program for Agriculture Science & Technology Development (Project No. 907002082012)’’ Rural Development Administration, Republic of Korea. This research was also supported by Basic Science Research Program through the National Research Foundation Korea funded by the Ministry of Education, Science and Technology (Project No. 2013R1A6A03022456). References Aaby, K., Skrede, G., & Wrolstad, R. E. (2005). Phenolic composition and antioxidant activities in flesh and achenes of strawberries (Fragaria  ananassa). Journal of Agricultural and Food Chemistry, 53, 4032–4040. Atkinson, C. J., Dodds, P. A. A., Ford, Y. Y., Le Miere, J., Taylor, J. M., Blake, P. S., et al. (2006). Effects of cultivar, fruit number and reflected photosynthetically active

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