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ISSN : 1598-5504(Print)
ISSN : 2383-8272(Online)
Journal of Agriculture & Life Science Vol.54 No.6 pp.1-10
DOI : https://doi.org/10.14397/jals.2020.54.6.1

Changes on the Fruit Quality of Strawberries (Fragaria × Ananassa Duch) in Response to Ripening Level, Storage Temperature, and Storage Period

Hyo-Gil Choi1, Nam-Jun Kang2,3,*
1Department of Horticulture, Kongju National University, Yesan 32439, Korea
2Department of Horticulture, Gyeongsang National University, Jinju 52828, Korea
3Institute of Agriculture & Life Science, Gyeongsang National University, Jinju 52828, Korea
*Corresponding author: Nam-Jun Kang Tel: +82-55-772-1915 Fax: +82-55-772-1919 E-mail: k284077@gnu.ac.kr
July 27, 2020 ; September 11, 2020 ; December 7, 2020

Abstract


In this study, we investigated the effects of the ripening level (50% and 100%), storage temperature (1°C and 10°C), and storage period (0, 7, and 14 days) on the fruit quality of the strawberry (Fragaria × ananassa Duch) cultivars “Arihyang” and “Kuemsil”, which are commonly grown for export in South Korea. Strawberry plants of each cultivar were grown in a plastic greenhouse, and fruit samples were harvested in January 2019 to evaluate the fruit hardness, gray mold rot, anthocyanin content, sugar content, and antioxidant activity. We found that “Arihyang” had a greater fruit hardness than “Kuemsil” across all storage periods excluding the day of harvest, and that fruit stored at 1°C had a greater hardness than fruit stored at room temperature (10 ± 2°C) for both cultivars. In incidence of gray mold rat, “Kuemsil” had a higher than “Arihyang”. The soluble solid content was highest at 7 days after harvest for both cultivars, with the exception of “Kuemsil” following storage at 1°C. The anthocyanin content was higher in “Arihyang” than in “Kuemsil” and was also greater in fruit that had been stored at room temperature due to the faster ripening time. Finally, the DPPH activity of fully ripened fruit tended to decrease as the storage period increased, while the ABTS activity was the same across all treatments. These findings demonstrate that “Arihyang” are more advantageous for long-term distribution as well as export than “Kuemsil”, and recommend that the two new cultivars of strawberry be cool stored at 100% ripening state and eaten within 7 days.



초록


    Rural Development Administration(RDA)
    PJ013834

    Introduction

    Strawberry (Fragaria × ananassa Duch, Rosaceae) is cultivated around the world, including in South Korea, where advanced technology for protected horticulture has resulted in strawberry cultivation by hydroponics representing 25% of the total strawberry growing area. The improvement of strawberry cultivation technology has increased the production of strawberry fruit which, in turn, has led to a steady increase in both the domestic distribution and export of this crop. However, a reduction in the strawberry cultivation area in South Korea has resulted in the annual revenue from strawberry production slightly decreasing from 1.36 billion US dollars in 2014 to 1.31 billion US dollars in 2016 (MAFRA 2017). Despite this, strawberry remains a very important component of the agricultural industry in South Korea, with the fruit being exported to many parts of the world, including Southeast Asia and Russia (Jeong et al., 2016). Consequently, two new strawberry cultivars (“Arihayng” and “Kuemsil”) were developed at the National Institute of Horticultural and Herbal Science and Geongsangnam-do Agricultural Research and Extension Services in South Korea to meet increasing export demands.

    Strawberry consumers generally prefer fruit that have a good morphological shape, taste, and contain high concentrations of functional phytochemicals, while fruit hardness is also an important characteristic for extending the storage period (Jeong et al., 2016;Kohyama et al., 2013). Strawberry fruit contain anthocyanins, which are naturally occurring polyphenol compounds that have received increasing attention due to their protective effects against many chronic diseases (Giampieri et al., 2014;Karaaslan & Yaman, 2017;Wallace, 2011). It has been reported that the amount of anthocyanin that is highly functional in ripe fruit depends on a number of environment factors (Faragher, 1983). In particular, the quality of strawberry fruit is greatly influenced by the postharvest management method, as well as factors such as the cultivar, temperature, and ripeness (Choi et al., 2013). In addition, strawberry fruit that are stored under high-temperature conditions during distribution after harvest produce more reactive oxygen species (ROS) and have a lower antioxidant enzyme activity (Vicente et al., 2006;Yang et al., 2017).

    Fruit hardness is a very important quality for the long-term storage of strawberry fruit, as this not only maintains the shape of the fruit but also prevents infection with pathogens (Salentijn et al., 2003). Consequently, strawberry fruit are harvested at an immature stage, despite the lower concentration of functional phytochemicals, in order to retain their hardness with the goal of safe distribution for export as well as domestic consumption (Park et al., 2012).

    Recently, two new strawberry cultivars "Arihyang" and "Kuemsil", which are exported to many countries including East Asia and Russia in the fresh fruit, and few studies had investigated postharvest changes in the basic quality of them (Yoon et al., 2020). Therefore, the aim of the present study was to assess the changes in the quality of these cultivars at different maturity stages, storage temperatures, and storage periods.

    Materials and Methods

    1. Fruit Sampling and Preparation of Fruit Extracts

    Our study was carried out at Kongju National University in South Korea from 2018 to 2019 using the strawberry cultivars “Arihyang” and “Kuemsil”. A total of 30 plants of each cultivar were transplanted on high-bench beds within a greenhouse and hydroponically cultivated by drip irrigation using Research Station for Floriculture and Glasshouse Vegetables (PBG, Aslmeer, Netherlands) nutrient solution [macro-elements (N: P: K: Ca: Mg: S = 12.5: 3.0: 5.5: 6.5: 2.5: 3.0 me·L−1), micro-elements (Fe: B: Mn: Zn: Cu: Mo = 1.12: 0.27: 0.55: 0.46: 0.05: 0.05 mg·L−1)] with electrical conductivities of 0.6 dS∙m−1 during the initial planting period, 0.8 dS∙m−1 during the budding period, and 1.0 dS∙m−1 after the blooming period, and hydrogen ion concentration (pH) = 5.5–6.5. The air temperature inside the greenhouse was kept above 8°C using supplemental electric heating.

    Strawberry fruit were sampled from each plant on January 2, 2019, when the fruit of the first flower cluster were either 50% ripened (R50) or fully ripened (R100). The average weight, length, and circumference of the harvested “Arihyang” fruits were 33±1g, 56±1mm, and 148±2mm, respectively (Table 1), and the average weight, length and circumference of the harvested “Kuemsil” fruits were 24.5±1g, 48±1mm, and 138±2mm, respectively (Table 2). The sample sizes of this experiment were 2 kilograms respectively by treatments on two maturity stages with different temperatures and for different periods. The harvested fruit in a container were then stored in a refrigerator (size: 65cmⅹ55cmⅹ130cm; floor area ratio: 40%; temperature: 0.5±1°C; relative humidity: 80±7%) or at room condition (temperature: 10±2°C; relative humidity: 40±10%) for 14 days. The fruit were sampled on the day of harvest and at 7 and 14 days after harvest to analyze the fruit quality. To measure the sugar content, anthocyanin content, and antioxidant activity of the fruit, 2 kilograms of fruit from each sample was homogenized and a 50-g aliquot was centrifuged at 16,000g for 30 min at 4°C (VS-24SMI; Vision Scientific Co. Ltd., Daejeon, Korea). The supernatant was then filtered through No. 2 Whatman filter paper and immediately placed in -70°C of freezer for storage.

    2. Measurement of Fruit Hardness and Gray Mold Rot Incidence

    The fruit morphological analysis of the fruits were obtained by weight, length and diameter. In addition, the hardness of R50 and R100 fruit was measured using 0.5mm diameter of fruit hardness tester (FHM-1, Takemura Electric Ltd., Tokyo, Japan). Three plastic boxes containing eight strawberries on each treatment were used to visually check for gray mold rot of fruit and determine the onset.

    3. Analysis of Sugars and Anthocyanin

    The soluble sugar contents of the thawed sample solutions were measured using a refractometer (PAL-1; ATAGO Co. Ltd., Tokyo, Japan). The anthocyanin contents of the fruit were analyzed using the method of Tonutare et al. (2014). Briefly, each frozen sample was thawed for 2 hours at room temperature and then extracted with 40 ml of ethanol (99%) and 0.1 M hydrochloric acid (85%:15%, v:v). A 3-ml aliquot of the resulting extract was then diluted in 5 ml of potassium chloride (pH 1.0) and sodium acetate (pH 4.5) buffers. After the diluted extracts had been reacted at room temperature for 30 minutes, their absorbance was measured using an ultraviolet-visible light (UVVIS) spectrophotometer (NEO-D3117; Neogen Ltd., Daejeon, Korea). The total anthocyanin content in the strawberry fruit was expressed as mg·100 g−1 fresh weight.

    4. Analysis of Antioxidant Activity

    The antioxidant activities of the thawed sample solutions were assayed using the 2,2-diphenyl-1-picrylhydrazyl (DPPH) and 2,2-azinobis-(3-ethylbenzothiazoline-6-sulfonic acid) (AB TS) assays, as modified by method of Choi et al. (2015). Each thawed extract was reacted with the DPPH radical in ethanol solution and changes in the color of the reaction sample after 100 minutes were measured at 517 nm using a NEO-D3117 UV-VIS spectrophotometer. The percentage of DPPH antioxidant activity was then determined according to the following formula: 100 − [(Absorbancesample – Absorbanceblank) × 100]/Absorbancecontrol. A 7.4 mM ABTS solution was reacted with 2.6 mM potassium persulfate, and the mixture was left in the dark at room temperature for 16 hours before use. The ABTS solution was then diluted with methanol to give an absorbance of 1.5 ± 0.02 at 734 nm. A 0.2-ml aliquot of the thawed fruit extract was added to 4 ml of the diluted ABTS solution, and the mixture was maintained at room temperature for 10 minutes. The absorbance of the mixture was then measured at 734 nm using a NEO-D3117 UV-VIS spectrophotometer, following which the percentage of ABTS antioxidant activity was calculated using the same formula as for DPPH.

    5. Statistical Analysis

    In this experiment, each treatment consisted of one repetition as 8 strawberry fruits in one container, and it was carried out in 3 replications. For the morphological characteristics of fruits such as fruit size and hardness and gray mold rot incidence by each treatment, after measuring all fruits in the container, the average value was set as one repeat value. The soluble sugar contents, phytochemicals, and antioxidant activity of fruits were analyzed in three repetitions as one repeat by extracted sample from homogenizing as all fruits of one container. Measurements of the soluble sugar contents, anthocyanin contents, and antioxidant activities of the fruit extracts were repeated three times. The difference between two groups by ripening were analyzed by t-test on harvest day. The effects of ripening and temperature were analyzed by two-way analysis of variance on measured 7 and 14 days after storage. The data were then statistically analyzed using analysis variance with Duncan’s multiple range test at p = 0.05 in SAS (SAS Institute Inc., NC, USA).

    Results and Discussion

    1. Morphological characteristics of strawberry fruit

    The morphological characteristics of the R50 and R100 strawberry fruit following storage at different temperatures and for different periods are shown in Tables 1 and 2 and Fig. 1 and 2. In “Arihyang” cultivar, the changes of morphological characteristics such as the weight, length, and circumference of fruit, which was only affected by temperature factor during 7 days of storage, but it was affected by both temperature and ripening factors after 14 days of storage (Table 1). On the other hand, the changes of morphological characteristics of “Kuemsil” cultivar was not significantly affected by temperature and ripening factors during 7 days of storage, however it was significantly affected by the temperature after 14 days of storage (Table 2). When strawberry fruits stored at room temperature during 14 days, R100 fruit of two strawberry cultivars showed a dramatic decrease by the order of weight, length and circumference (“Arihyang” was 16%, 9%, 8%, and “Kuemsil” was 23%, 12%, 9% respectively) as well as especially the storage temperature was significantly affected on the loss of weight and reduction of size in R100 fruit of “Kuemsil” (Fig. 1). Strawberry fruits differently lose weight due to difference in moisture loss depending on the storage temperature and method during storage period (Velickova et al., 2013;Zhang et al., 2018). We confirmed that not only the storage methods and temperatures identified in previous studies, but also difference of strawberry cultivars play an important factor in quality change after postharvest.

    For both two cultivars, the R50 fruit that were stored at 1°C remained in an unripe condition and maintained their fresh shape even after 14 days of storage, whereas those that were kept at room temperature almost attained the full ripening condition after 7 days of storage. Furthermore, when the R100 fruit were stored at 1°C, the color of their skin changed to a vivid red as the storage period increased. There was a greater reduction in the volume of the fruit following storage at room temperature compared with storage at 1°C for both ripening levels (Fig. 2).

    In addition, the condition of the R100 fruit which were stored at room temperature deteriorated to such an extent that these could no longer be distributed to the market after 14 days of storage due to the occurrence of gray mold rot, which had a higher incidence ratio on the R100 fruit than the R50 fruit following storage at room temperature and on “Kuemsil” than on “Arihyang” (Fig. 3). There is reported that the incidence of gray mold (Botrytis cinerea) disease was predominantly 20°C to 25°C, 10°C higher than 35°C, and rarely grew below 5°C and above 35°C (Czaja et al., 2016). Another study showed that the percentage of incidence of gray mold of strawberry fruit stored at 21°C was 69-100%, and 0-17% at 4°C (Jeon et al., 2017). The other study reported that strawberry fruit did not develop gray mold rot when stored at 5°C and 10°C for 10 days (Choi et al., 2013), these results are similar to the findings of the present study. However, our results differed from those of Nunes et al. (2012), who found that the incidence ratio of gray mold rot on strawberry fruit was lower at 10°C than at 4°C under controlled-atmosphere storage conditions using CO2. Some studies reported that treatments of various substance can control to some extent strawberry gray mold decay after harvest (Feliziani et al., 2015;Saavedra et al., 2017). However, Feliziani & Romanazzi (2016) are similar to our findings, who suggested that the best protection of gray mold rot of strawberry fruit after harvest is to be stored at low temperatures at which gray mold cannot be activated.

    Fruit hardness is an important indicator in the control of distribution and sale of strawberry after harvest. Changes in the fruit hardness of “Arihyang” and “Kuemsil” at different ripening levels, storage temperatures, and storage periods are shown in Fig. 3. On the day of harvest, the fruit hardness varied with the level of ripening but did not significantly differ between the cultivars. However, as the storage period increased, there was a significant difference in fruit hardness between all treatments. The fruit hardness of the R50 fruit of both cultivars gradually increased excluding “Kuemsil” stored at room temperature condition. This is considered to be a phenomenon caused by shrinkage of fruit tissue due to a decrease in moisture, which occupies most of the weight on a fruit, while storing strawberries. It is similar that as persimmons before completely ripe, they are dry and become dried persimmons, moisture decreases and tissue shrinks, increasing hardness (Kang et al., 2004). On the other hand, in the case of R50 fruit of “Kuemsil” stored at room temperature, there was also a shrinkage of the tissue due to the decrease in moisture, but it is conjectured that the hardness decreasing was more affected due to the various environmental conditions of external room temperature than that the “Arihyang” cultivar. While that of the R100 fruit steadily decreased during storage at room temperature. Furthermore, “Arihyang” had a higher fruit hardness than “Kuemsil” after 14 days of storage. These findings indicate that both the storage conditions and cultivar affect the fruit hardness and thus the quality of the fruit for storage and export. These results are similar to those of previous studies, which have shown that β-galactosidase activity is high at the end of fruit maturity, which causes the cell walls to break down, resulting in a very low hardness of R100 fruit (Ahmed & Labavitch, 1980;Choi et al., 2013;Jiang et al., 2019). Furthermore, the results of our experiment showed that strawberry fruit were harder following storage at 0°C, with a moderate increase in hardness over time. These results are in agreement with the findings of Smith (1992). Also, some of the studies reported that the fruit hardness increased when the fruit was precooled after harvesting (Aksel et al., 2005;Maezawa & Akimoto, 1995).

    2. Soluble solid contents and anthocyanin

    Changes in the sugar contents of the fruit of “Arihyang” and “Kuemsil” at different ripening levels, storage temperatures, and storage periods are shown in Fig. 4. In the case of “Kuemsil”, the sugar content of the R100 fruit that were stored at room temperature was higher at the time of harvest and after 7 days of storage than after 14 days of storage due to respiration and physiological degeneration, whereas the sugar content of the R50 fruit increased continuously until 14 days of storage regardless of the storage temperature. In addition, “Kuemsil” fruit generally had a higher sugar content than “Arihyang” fruit, which contrasts with the pattern that was observed for fruit hardness. In an experiment of strawberry storage during 6 days, which reported that total sugars of fruit were significantly increased in storage of 16°C compared with 6°C as well as the levels of total sugars were statistically different among the strawberry cultivars (Cordenunsi et al., 2005). These of this study is similar to our results related total sugar analysis. Our findings indicate that biochemical changes in the strawberry fruit were affected by both the cultivar and the maturation level, with the sugar content gradually increasing during maturation, which supports the previous findings of Moing et al. (2001).

    Anthocyanins are known to have antioxidant activity and have been reported to vary in content depending on the storage condition (Muche et al., 2018). The anthocyanin contents of the fruit of “Arihyang” and “Kuemsil” at different ripening levels, storage temperatures, and storage periods are shown in Fig. 4. The fruit of both cultivars had an anthocyanin content of approximately 10 mg·100 g−1 immediately after harvest, with no significant difference between the R50 and R100 fruit. However, the anthocyanin content in the “Arihyang” fruit increased rapidly over the first 7 days of storage, with the exception of the R50 fruit that were stored at 1°C. In particular, the R100 fruit that were stored at room temperature exhibited a four-fold increase in anthocyanin content after 7 days of storage compared with levels at the time of harvest. The anthocyanin content of “Arihyang” fruit then decreased as the storage period extended beyond 7 days. By contrast, the anthocyanin content of “Kuemsil” fruit slowly increased until 14 days after storage, with the exception of the R50 fruit that were stored at 1°C. The anthocyanin content of the fruit was also affected by the storage conditions, but the amount of variation between cultivars was much greater. The observed change in anthocyanin content in response to storage conditions was similar to the morphological change in the red skin (Figs. 1 and 4), which is analogous to the findings of (Andersen et al., 2004), who reported that the anthocyanin pigments in strawberry contain large amounts of pelargonidin- 3-glucoside and are an important component of the red skin pigmentation.

    3. DPPH and ABTS scavenging activity

    Highly toxic ROS are continuously produced in horticulture crops as byproducts of aerobic metabolism but can be rapidly detoxified through various enzymatic and nonenzymatic mechanisms (Apel & Hirt, 2004). The antioxidants that neutralize ROS in plants are mainly metabolites of phytochemicals such as anthocyanin, and the DPPH and ABTS assays are widely used to confirm their activities (Dudonne et al., 2009). The DPPH free radical scavenging activity of the strawberry fruit shortly after harvest did not significantly differ between the cultivars or maturity levels, and there was little change in the DPPH activity of the strawberry fruit as storage progressed (Fig. 5). However, the DPPH activity of the R100 fruit of both cultivars significantly decreased as the storage period increased. These findings are similar to those of Kalt (2005), who reported that the antioxidant capacity of fruit decreases during storage, which we presume is due to respiration and aging of the R100 fruit during long-term storage at room temperature. By contrast, we found that the ABTS activity of the fruit was >90% for all storage periods, with no significant difference between treatments (Fig. 5), which supports the findings of Kalt (2005), who showed that the ABTS activity of strawberry fruit is not affected by the cultivar or environmental conditions during storage, but contrasts with those of Piljac-Žegarac & Šamec (2011), who reported that the ABTS value of strawberry fruit slightly changes during storage at temperatures of 4°C and 25°C.

    Conclusions

    Based on these findings from our study, the following conclusions can be drawn. After harvesting or purchasing strawberries, there is better to store in a low temperature of below 5°C than in a room temperature of above 10°C in order to prevent external morphological changes such as the weight loss of the fruit and the occurrence of grey mold.

    In addition, considering the best taste and nutrition of new strawberry cultivars such as “Arihyang” and “Kuemsil” as well as most of strawberry cultivars, we recommend that a farmer need to harvest strawberry fruit from ripening above 80% and a distributor need to sell as its’ refrigerated and consumers should eat within 7 days after harvest day with reference to the agriculture product resume system.

    We confirmed that “Arihyang” strawberry cultivar in South Korea, which have been specifically bred for export to more than 10 countries, it is the superior cultivar than “Kuemsil” strawberry cultivar for export as it retained it’s a good morphological characteristics during long-term storage. And “Arihyang” strawberry cultivar had a lower incidence of gray mold rot as well as which was high quality fruit in terms of fruit hardness and anthocyanin content.

    Acknowledgments

    This study received financial assistance from Rural Development Administration of Korea (Project No. PJ013834).

    Figures

    JALS-54-6-1_F1.gif

    Loss ratio of weight and reduction rate of size of fruit of the strawberry (Fragaria × ananassa) cultivars “Arihyang” and “Kuemsil” during storage at different ripening levels and storage temperatures. A: “Arihyang”; K: “Kuemsil”; 50: 50% ripening; 100: full ripening; CS: cold storage at 1°C; RS: storage at room temperature (10 ± 2°C).

    JALS-54-6-1_F2.gif

    External quality of fruit of the strawberry (Fragaria × ananassa) cultivars of “Arihyang” (upper) and “Kuemsil” (lower) during storage at different ripening levels and storage temperatures. The plastic box size for storing strawberries is 160mm x 110mm. 50: 50% ripening; 100: full ripening; CS: cold storage at 1°C; RS: storage at the room temperature (10 ± 2°C).

    JALS-54-6-1_F3.gif

    Incidence ratio of gray mold rot (upper) and hardness (lower) of fruit of the strawberry (Fragaria × ananassa) cultivars “Arihyang” and “Kuemsil” at different ripening levels, storage temperatures, and storage periods. Three plastic boxes containing eight strawberries were used to visually check for gray mold rot of fruit. A: “Arihyang”; K: “Kuemsil”; 50: 50% ripening; 100: full ripening; CS: cold storage at 1°C; RS: storage at room temperature (10 ± 2°C). Vertical bars represent standard error (n = 3). XP values were determined by t-test measured on harvest day. YP values were determined by two-way ANOVA measured on 7 days of storage. ZP values were determined by two-way ANOVA measured on 14 days of storage. Different lower case letters within each storage period indicate significant differences between the means (Duncan’s multiple range test, p < 0.05).

    JALS-54-6-1_F4.gif

    Soluble sugar contents (upper) and anthocyanin contents (lower) of fruit of the strawberry (Fragaria × ananassa) cultivars “Arihyang” and “Kuemsil” during storage at different ripening levels and storage temperatures. A: “Arihyang”; K: “Kuemsil”; 50: 50% ripening; 100: full ripening; CS: cold storage at 1°C; RS: storage at room temperature (10 ± 2°C). Vertical bars represent standard errors (n = 10). XP values were determined by t-test measured on harvest day. YP values were determined by two-way ANOVA measured on 7 days of storage. ZP values were determined by two-way ANOVA measured on 14 days of storage. Different lower case letters within each storage period indicate significant differences between the means (Duncan’s multiple range test, p < 0.05).

    JALS-54-6-1_F5.gif

    DPPH free radical scavenging activity (upper) and ABTS radical cation decolorization activity (lower) of fruit of the strawberry (Fragaria × ananassa) cultivars “Arihyang” and “Kuemsil’ during storage at different ripening levels and storage temperatures. A: “Arihyang”; K: “Kuemsil”; 50: 50% ripening; 100: full ripening; CS: cold storage at 1°C; RS: storage at room temperature (10 ± 2°C). XP values were determined by t-test measured on harvest day. YP values were determined by two-way ANOVA measured on 7 days of storage. ZP values were determined by two-way ANOVA measured on 14 days of storage. Vertical bars represent standard errors (n = 3). Different lower case letters within each storage period indicate significant differences between the means (Duncan’s multiple range test, p < 0.05).

    Tables

    Morphological characteristics of fruit of the strawberry (Fragaria × ananassa) cultivar “Arihyang” at different ripening levels, storage temperatures, and storage periods

    Morphological characteristics of fruit of the strawberry (Fragaria × ananassa) cultivar “Kuemsil” at different ripening levels, storage temperatures, and storage periods

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