Enhancement of quality and antioxidant metabolism of sweet cherry fruit by near-freezing temperature storage

Postharvest Biology and Technology 147 (2019) 113–122

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Enhancement of quality and antioxidant metabolism of sweet cherry fruit by near-freezing temperature storage Handong Zhao, Bangdi Liu, Wanli Zhang, Jiankang Cao, Weibo Jiang

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College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, PR China

ARTICLE INFO

ABSTRACT

Keywords: Sweet cherry Near-freezing temperature storage Postharvest quality Antioxidant enzyme Reactive oxygen species Antioxidant capacity

Near-freezing temperature storage (NFTS) is a novel method to inhibit quality loss of fresh fruit. However, little information is available on NFTS delaying the onset of senescence in sweet cherry (Prunus avium L.) fruit and regulating the changes on antioxidative enzymes participated in the balancing of reactive oxygen system (ROS). Fruits were stored at NFT (between super-cooling point and freezing point), 0 °C and 5 °C, respectively, until fruits exhibited visually rot (sampled every twenty days). NFTS effectively slowed senescence process in sweet cherry fruit, as indicated by extending storage duration and improving the changes of firmness, anthocyanins, ion leakage, peel color and sugars content. Moreover, fruit stored at NFT had higher levels of ascorbic acid, phenolics and organic acids and lower accumulation of carotenoids, malondiadehyde, hydrogen peroxide (H2O2) and superoxide radical (O2•¯). Additionally, NFTS maintained membrane integrity and prevented fresh browning of fruit by enhancing the activities of superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX) and gluta thione reductase (GR) and inhibiting the activities of guaiacol peroxidase (POD), polyphenol oxidase (PPO) and lipoxygenase (LOX). Furthermore, NFTS fruit exhibited higher level of antioxidant capacity as measured by radical scavenging activity and reducing power at the end of storage. These results indicate that the activities of antioxidant enzymes to scavenge superoxide anions and H2O2 during NFTS was implicated in the maintenance of membrane integrity, which might be a part of the mechanism associated with the delay of senescence in sweet cherry fruit.

1. Introduction Sweet cherry (Prunus avium L.) has become one of the most important non-climacteric fruits worldwide for its satisfaction of quality attributes (Habib et al., 2015). Moreover, sweet cherry is becoming more and more popular due to its bioactive compounds with antioxidant characteristics, generally including polyphenols, vitamins, anthocyanins and carotenoids (Gonçalves et al., 2004; Serradilla et al., 2012; Usenik et al., 2008). Previous study has proved that cherry consumption was related with a lessening of several diseases, including cancer, cardiovascular, diabetes and inflammatory diseases, as a result of a decline in oxidant stress, tumour suppression, inflammation and glucose control (Mccune et al., 2011). However, sweet cherry fruit is highly perishable owing to softening rate (Meheriuk et al., 1995) as a result of the high rate of transpiration and respiration, mechanical bruises and high susceptibility to fungal infections (Alique and Zamorano, 2005; Ceponis et al., 1987), which dramatically influence their storability and marketing acceptability after harvest. Basically, the main postharvest treatment to reduce the

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quality loss and extend storability of sweet cherry fruit is cold storage (Petriccione et al., 2015), but traditional cold storage method generally causes some physiological disorder, such as surface pitting and anthocyanins degradation (Correia et al., 2018; Wani et al., 2014). Nearfreezing temperature (NFT), within the range of minimal non-frozen temperatures, is determined by freezing curve of the individual material (Supplementary material Fig. S1D), which originally been used to store fresh fish and animal organs (Okamoto et al., 2008; Zhu et al., 2016). Recent research exhibited that nectarine and apricot fruits also preferably preserved physiological and commercial qualities with the near-freezing temperature storage (NFTS) (Zhao et al., 2018; Fan et al., 2018). In our study, we have found NFTS could reduce the decay rate, delay the ripening process and maintain the higher content of bioactive compounds and antioxidant activity as compared with the traditional cold storage, which might associate to the changes in relative enzyme activity. Reactive oxygen species (ROS), such as hydrogen peroxide (H2O2) and superoxide radical (O2%−), are inevitably originated in plant cell as a consequence of normal metabolism, which are mainly produced in

Corresponding author. E-mail address: [email protected] (W. Jiang).

https://doi.org/10.1016/j.postharvbio.2018.09.013 Received 19 June 2018; Received in revised form 12 September 2018; Accepted 14 September 2018 0925-5214/ © 2018 Elsevier B.V. All rights reserved.

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reactions catalyzed by oxidase and lipoxygenase (LOX). Moreover, the producing and scavenging systems, including both non-enzymatic antioxidant and enzymatic mechanisms, are predicted the ROS content in plant cell (Apel and Hirt, 2004). Non-enzymatic compounds of sweet cherry fruit mainly include phenolics, anthocyanins, carotenoids and ascorbate acid, while the antioxidant enzymes, such as superoxide dismutase (SOD), catalase (CAT), peroxidase (POD) and ascorbate peroxidase (APX), are principal active free radical scavenging enzymes (Valverde et al., 2015). SOD converts the O2%− free radical to O2 and H2O2, then the CAT catalyses the decomposition of H2O2 to water and oxygen. Additionally, ascorbate and H2O2 are transformed to water and dehydroascorbate by APX, and H2O2 can be also reduced to water by using POD and phenols (Tareen et al., 2012). Although the presence of these antioxidant systems is dynamic and efficient, plant cells are still occurred by oxidative damages on account of uncontrolled production or incompetent scavenging of ROS. Thus, the process of fruit ripening and senescence associates with ROS accumulation (Hodges, 2004), so the content of antioxidant compounds and the activities of antioxidant enzymes could affect the fruit storability (Mondal et al., 2009; Kumar, 2014). However, there is no literature about the effect of NFTS on the behavior of antioxidant enzymatic systems and membrane integrity in fresh fruit. The objective of our study was to research the effect of NFTS on antioxidant enzymatic system and membrane metabolism of sweet cherry fruit and to understand the inter-relationship between NFTS and oxidative stress as well as the association with postharvest senescence.

freezing point and super-cooling point of sweet cherry fruit were determined based on the biological freezing curve. The freezing temperature curve and the NFT determination of sweet cherry were exhibited in supplementary material (Fig. S1C and D). The curve displayed that the super-cooling point and freezing point of fruit were –3.3 °C and–2.8 °C, respectively (Fig. S1D). To avoid freezing damage, the NFT of sweet cherry fruit was controlled at −3.0 ± 0.1 °C which is slight higher than supper-cooling point. Previous research confirmed that there was a high negative correlation between soluble solids and freezing point (Jie et al., 2003), and the higher levels of soluble sugars in fruit prevent water transferring out of the cells, which enhance the osmotic potential and make it difficult to form the ice crystals. Thus, higher soluble solids could enhance the NFT tolerance and osmotic potential of fruit. 2.2. Evaluation of firmness, ascorbic acid, total anthocyanins, total caroteniods and color changes Fruit firmness was measured as penetration force on the fruit flesh. A penetrometer (Effegi pressure tester, Facchini 48011, Alfonsine, Italy) with a 3.5 mm probe was used to test the firmness and the results were expressed in N. Ascorbic acid was extracted and analyzed by Xi’s method (Xi et al., 2017). Anthocyanins content was estimated by a pHdifferential method (Albishi et al., 2013) and expressed as cyanidin-3glucoside equivalent (CGE) per kilogram of fresh weight (molar extinction coefficient of 26,900 L cm−1 mol−1 and molecular weight of 449.2 g mol−1). Absorbance measurements were conducted at 520 and 700 nm. Total carotnoids were extracted according to previous method (Giménez et al., 2016). The peel color change was determined using a reflectance spectrophotometer (Model NF333, Nippon Denshoku Industries, Tokyo, Japan). For color measurement, thirty fruits were randomly picked from each replicate, and color was expressed according to the CIE Lab system (a-red/green and b-yellow/blue), and the value of a, b were converted to Hue angle (a relative ratio of the yellow intensity to red intensity) and Chroma (an indicator of redness) [Hue angle (tan−1 (b/ a)) and chroma, a measure of color clarity (a2+b2)1/2].

2. Materials and methods 2.1. Plant material and NFT determination Sweet cherry (Tieton) was obtained from an experimental orchard in Beijing at commercial maturity stage (firmness was about 3.9 N and SSC was about 18.3%). Fruit trees were maintained with standard cultivation, fertilizer, herbicide and pesticide practices. Fruits, with uniformity in shape, size, color and physical integrity without visual defects, were harvested randomly and transported to the laboratory immediately. Fruit was pre-cooled in an experimental temperaturecontrolled wind tunnel at 5 °C for 24 h. After pre-cooling, fruits were randomly separated into 5 °C, 0 °C or NFT (﹣3..0 ± 0.1 °C) for the sweet cherry group × 3 replications = 9 lots (5 kg per lot). All fruits were stored with a relative humidity (RH) of 90 ± 2% in darkness. Samples were removed on every twenty days during storage to evaluate the physiological and antioxidant capacity changes. 50 fruits (about 500 g fruit flesh) were used in each replicate (per lot), and there were about 150 fruits used for each sampling date in each temperature group for 3 replicates. Flesh sample was immediately used or frozen in liquid nitrogen and stored at –80 °C. All experiments were performed in triplicate. To ensure the storage temperature precise, the new storage equipment, including refrigerated storage system, microcontrollers, temperature sensors, alarm device and temperature-controlling, was designed (Fan et al., 2018). The temperature control mode could display and set the box storage temperatures in real-time (Fig. S1 A). Once the temperature exceeded the setting range, the temperature control mode could regulate the fans or electric heater to keep the temperature within the designed parameters (Fig. S1B). To confirm the biological freezing point and super-cooling point of sweet cherry fruit, previous method (Jie et al., 2003) was modified. After calibrated the thermocouple by the mixture of 0 °C water and ice, twenty fruits were selected randomly to determine the freezing curve by the HP34970 A data collector. Then, to obtain biological freezing curve, samples with thermocouples were situated in a freezer (−20 °C) and the temperature data was recorded every 10 s. The biological

2.3. Analysis of sugars, organic acids and phenolic compounds Extraction and determination of sugars was performed according to previous condition with some modifications (Fan et al., 2017). 1 g sample was ultrasonic extracted at 30 °C for 1 h and centrifugated at 10,000g for 20 min. Sugar compounds, including fructose, sorbitol, glucose and sucrose, were identified and quantified by comparing relative retention time and peak area of standard substance (Fig. S2). For testing organic acids, 1 g fresh sample was ground in 20 mL deionized water and shaken at room temperature for 1 h. The organic acids was analyzed according to (Fan et al., 2017) method, and identified and quantified by comparing relative retention time and peak area of samples and standard substances (Fig. S3). To evaluate phenolic compounds, a HPLC method (Liu et al., 2015), with a Shimadzu liquid chromatograph, was used (Fig. S4). To test soluble solid content (SSC), 50 fruits from each replication were randomly selected. SSC was tested by a digital refractometer (PR101, Spectrum Technologies, Plainfield, IL), and results were expressed in percentage (%). Titratable acid (TA) was determined by titrating 25 mL of cherry juice to pH 8.5 with 0.1 mol L−1 NaOH, and results were expressed as the percentage of malic acid. To investigate total phenolic compounds, sample was extracted from 8.0 g frozen sweet cherry flesh as previous research (Pérez-Jiménez and Saura-Calixto, 2005). Total phenolics (TP) concentration was measured by the FolinCiocalteu method and expressed as gram gallic acid equivalents per kilogram fresh weight.

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2.4. Assessment of enzyme activities and total soluble protein content

2.6. The production of H2O2 and O2%−

SOD (EC 1.5.1.1) was extracted from 2 g of frozen flesh powder with 10 mL of 50 mmol L−1 sodium phosphate buffer (pH 7.5) at 4 °C. After 20 min centrifugation at 10,000g for, the supernatant was used to test SOD activity by previous study (Sgherri et al., 2015). One unit of SOD activity is defined as the amount of enzyme that causes 50% inhibition of nitroblue tetrazolium (NBT). CAT (EC 1.11.1.6) activity was tested following the previous research (Chance, 1995). 2 g tissue and 5 mL of 50 mmol L-1 sodium phosphate buffer (pH 7.0) was homogenized to prepare enzyme extract. To determine the CAT activity, 0.2 mL enzyme preparation was added into 50 mmol L−1 sodium phosphate buffer (pH 7.0) containing H2O2 as a substrate. One unit of CAT activity was designated as the amount of enzyme that decomposes 1 μmol of H2O2 per minute at 30 °C. APX (EC 1.11.1.11) activity was evaluated following previous report (Nakano and Asada, 1981). The extract was brought from 2 g tissue was homogenized with 7 mL of 50 mmol L−1 sodium phosphate buffer (pH 7.0). The reaction included 0.2 mL enzyme liquid, 0.1 mL 9 mmol L−1 AsA, 50 μL of 30% (v/v) H2O2 and 3 mL 100 mmol L−1 sodium phosphate buffer (pH 7.0). One unit of APX was described as the amount of enzyme that oxidised 1 μmol ascorbate per minute. Glutathione reductase (GR, EC 1.6.4.2) activity was tested following previous method (Thorne, 1988). GR activity was tested by monitoring glutathione-dependent oxidation of NADPH at 340 nm. The mixture, containing 3 mmol L−1 NADPH, 5 mmol L−1 MgCl2 and 10 mmol L−1 oxidised glutathione, was prepared. One unit of GR was explained as an increase of 0.001 in absorbance per minute under the assay conditions. To prepare POD (EC 1.11.1.7) and polyphenol oxidase (PPO, EC 1.10.3.2) extract, 3 g powders were homogenized with 15 mL 50 mmol L−1 sodium phosphate buffer (pH 7.0) containing 5% (w/v) PVPP for POD and PPO. POD activity was determined according to previous method (Jing et al., 2013). One unit of POD activity is defined as the amount of enzyme that causes an increase in absorbance of 0.01 at 470 nm per minute. Additionally, PPO activity was measured following the method of (Kumar et al., 2008). One unit of enzyme activity is defined as the amount of enzyme that causes an increase in absorbance of 0.001 at 420 nm per minute. For LOX (EC 1.13.11.12) measurement, 5 g flesh tissue was homogenized with 5 mL of 50 mmol L−1 Tris-HCl (pH 8.0) containing 10 mmol L−1 KCl, 500 mmol L−1, sucrose and 0.5 mmol L−1 phenylmethylsulfony fluoride. LOX activity was tested according to previous method (Todd et al., 1990). One unit of LOX was described as the amount of enzyme which induces an increase in absorption at 234 nm of 0.01 min−1 at 25 °C when linoleic acid is used as the substrate. The total soluble protein was estimated by Bradford method (Bradford, 1976), with bovine serum albumin as a standard. All the enzyme activities were expressed as units per milligram of protein.

H2O2 content was tested followed by previous method (Patterson et al., 1984) with some modification. Sweet cherry flesh tissue (6 g) was homogenized in 5 mL of cold acetone and centrifuged at 10,000g and 4 °C for 30 min. 1 mL supernatant was mixed with 0.1 mL of 22 mmolL−1 titanium sulphate and 0.2 mL ammonia, and the mixture centrifuged at 10,000 g and 4 °C for 15 min. Then, the pellets were dissolved in 3 mL of 1 mol L−1 sulfuric acid and centrifuged for 15 min at 10,000 g. H2O2 production was tested using H2O2 as a standard and expressed on a fresh weight basis as mol kg−1. O2%− production was tested in 5 g of sweet cherry flesh tissue according to a modified method (Wang and Luo, 1990). NaNO2 as a standard was used to calculate the O2%− production, and the results expressed as μmol kg−1 h−1. 2.7. Non-enzymatic antioxidant activity assay The antioxidant activities of pulp of sweet cherry was tested using DPPH and ferric reducing antioxidant power (FRAP), with 3 g fresh sample. For test radical scavenging activity, 200 μL sample extract was mixed with 4 mL of DPPH radical (300 μM). After incubated at 25 °C for 60 min, the absorbance of mixture at 517 nm was recorded (Ibrahim et al., 2012). Aqueous solution of Trolox was used for calibration, and the results were expressed as mmol kg−1 fresh weight basis. FRAP was performed according to previous method (Benzie and Strain, 1996), and the antioxidant ability was tested by a standard curve using FeSO4. FRAP results were showed as millimoles FeSO4 per kilogram fresh weight. Total antioxidant activity (TAA), including hydrophilic (H-TAA) and lipophilic (L-TAA) compounds, was tested following a previous method (Wang et al., 2015a,b). The results of H-TAA and L-TAA are showed as milligram Trolox equivalent (TEs) per kilogram fresh weight. 2.8. Statistical analysis The antioxidant relevant data of three temperatures storage randomly dispersed in the main plots and storage duration were randomly dispersed in the sub plots. Correlations among the antioxidant parameters and NFTS were analyzed by Spearman’s correlations (p < 0.05 and p < 0.01) with SPSS version 20 Windows (SPPS Inc., Chicago, Illinois, USA). All examinations were completely randomized with three replicates and subjected to analysis of variance (ANOVA). In all cases, significant differences were performed by Duncan’s multiple range tests (p < 0.05). 3. Results and discussion 3.1. NFTS enhanced firmness, the content of ascorbic acid, total anthocyanins and total caroteniods and color changes

2.5. Measurements of ion leakage and malondialdehyde (MDA) concentration

For consumer acceptance and storability, firmness is an important quality characteristic of sweet cherry (Bai et al., 2011). Fruit firmness at harvest was 3.8 ± 0.3 N and noticeably decreased at the end of storage reaching final values of 2.3 ± 0.4 N and 1.6 ± 0.3 N in 0 °C and 5 °C, respectively, and significantly higher, 2.9 ± 0.4 N in NFTS (Fig. 1A). Previous research showed enzymatic degradation of the middle lamella of cell walls and respiration rate leads to softening (Wei et al., 2011). Therefore, quality of sweet cherry could be improved in the NFTS, which could reduce the rate of respiration and degradation of cell wall (middle lamella), maintain the cellular membrane integrity and alleviate softening process of the fruit. Sweet cherry is considered as a healthy fruit due to its bioactive compounds, such as ascorbic acid and anthocyanins. The content of

20 disks (5 mm diameter) of flesh tissue of 20 fruits were used to determine the ion leakage. The disks were steeped in doubly distilled water in glass vials for 60 min and the solution conductivity was tested. Then the disks were boiled for 30 min and cooled to room temperature, so the total conductivity was collected. Ion leakage was displayed as relative conductivity, (conductivity of tissue solution/total conductivity) ×100%. MDA accumulation was evaluated by the thiobarbituric acid reactive substances assay (Hodges et al., 1999). 2 g fresh tissue and 5 mL 30 mmol L−1 trichloroacetic acid were homogenized, and then mixture was centrifuged at 10,000×g for 10 min at 4 °C. The concentration of MDA was expressed as μmol kg−1 fresh weight. 115

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Fig. 1. Effect of the NFTS on firmness (A), ascorbic acid content (B), total anthocyanins content (C), carotenoids content (D), hue angle (E), chroma (F) and color changes(G) of ‘Tieton’ sweet cherry fruit. Data are expressed as the mean ± SE (n = 3). Vertical bars represent the standard errors of the means.

ascorbic acid of sweet cherry decreased rapidly at 0 °C and 5 °C groups during storage, while the NFTS delayed the decrease (Fig. 1B). After one hundred days, NFTS maintained 78.5% of the initial ascorbic acid concentration. Ascorbic acid would decline noticeably in sweet cherry during storage (Tian et al., 2004). In this sense, the NFTS improved ascorbic acid content and nutritional quality of sweet cherry. Changes in anthocyanins were shown in Fig. 1C. Total anthocyanins increased initially and followed by a decreasing at 0 °C and 5 °C groups throughout storage duration, but NFTS displayed a slightly continuous increasing and maintain the higher level in 100 d (Fig. 1C). The anthocyanins changes have been related to fruit ripening process and correlated with color parameters (Serrano et al., 2009), but the high oxidative activity of polyphenoloxidase and increasing pH might decline the anthocyanin content of cherries fruit at refrigerated temperature storage (Conte et al., 2009). Total carotenoids at harvest (39.0 ± 3.0 mg kg−1) increased significantly during storage at all temperatures, while the NFTS maintained a lower level compared with 0 °C and 5 °C storage (Fig. 1D). This result was similar with the previous study (Fan et al., 2018), and the increasing carotenoid level was related to the ripening process in both yellow and red-purple cultivars (Valero et al., 2011). So the NFTS could delay ripening process and prevent biological disorder of sweet cherry. Hue angle and chroma are the important parameters to evaluate fruit color changes, and both of them exhibited the similar trend during storage period (Fig. 1E and F). During the storage, the values of both hue angle and chroma showed sustained decrease, while NFTS could maintain the higher levels at the end of storage. Color changes during sweet cherry storage are mainly related to cultivars and the contents of anthocyanins and their profile (Giménez et al., 2017). Moreover, hue angle H° is based on maturity stage, such as full bright red (H° = 16.9) and dark red (H° = 11.85) (Crisosto et al., 2002), so the result revealed that NFTS could avoid fruit over-ripening and improve the appearance in the end (Fig. 1G).

decreased continuously at 0 °C and 5 °C, while the content of NFTS maintained the higher level. With fruit ripening or storage, the fructose may transform to glucose and other monosaccharide. SSC exhibited an initial increase and followed by a decreased during the storage at 0 °C and 5 °C (Table 1), while NFTS showed a continuously slight increasing. SSC changes could be attributed to starch transformation to sugar, to the cell wall hydrolysis, but, on the other hand, the decrease might relate to respiration and sugars conversion (Petriccione et al., 2015). Low temperature generally induced the starch conversion to reducing sugars (Martins et al., 2005), and the results exhibited fruit stored at NFT could reduce consumption of soluble sugars. So this phenomenon indicated the NFTS could effectively improve the SSC of sweet cherry during long time shipping or storage. Malic and citric acids were all detected in Tieton sweet cherry, and its predominant organic was malic acid which is agreement with Usenik et al. (2008). The content of malic acid and TA showed continuously decrease with increasing storage duration at 0 °C and 5 °C, while NFTS delayed the decrease and retained higher level as compared with 0 °C and 5 °C storage (Table 1). The higher TA loss at 0 °C and 5 °C might be associated to the use of organic acids as substrates for respiration metabolism (Díaz-Mula et al., 2012). The lower TA loss in NFTS was also reported in other researches on nectarine and apricot (Fan et al., 2018; Zhao et al., 2018). Neochlorogenic acid was the mainly phenolic acid in Tieton sweet cherry, and it decreased in the whole storage duration (Table 1). Interestingly, with respect to TP, levels increased significantly in all temperatures storage and therefore decreased until the end of storage. However, the concentration of TP was significantly higher at NFT than at 0 °C and 5 °C at the end of storage. The change of TP could be affect by several factors, such as ripening stage and cultivars, so NFTS delays the change in fruit TP concentration. 3.3. Effect of the NFTS on enzyme activity

3.2. NFTS improved the content of sugars, organic acids and phenolic compounds

During this storage, some enzymes, involving oxidative stress, browning and membrane damage, induce corresponding biochemical and physiological reactions. Thus, the changes of antioxidant system, which could affect membrane integrity metabolism and fruit senescence process, were estimated during NFTS.

Glucose, fructose, sucrose and sorbitol were the principle soluble sugars and sugar alcohol in Tieton sweet cherry (Table 1). Glucose and was found to have the highest content, followed by fructose, confirming the result of Usenik et al (2008). During the storage, fructose content 116

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Table 1 NFTS improved the content of sugars, organic acids and phenolics. Temperture

NFT

0 °C

5 °C

Storage time (days)

Glucose (g kg−1)

Fructose (g kg−1)

Sucrose (g kg−1)

Sorbitol (g kg−1)

SSC (%)

Malic acid (g kg−1)

Citric acid (g kg−1)

TA (%)

Neochlorogenic acid (mg kg−1)

Chlorogenic acid (mg kg−1)

0

75.2 aa

65.2 a

5.2 a

32.3 a

18.3 a

5.9 a

0.20 a

0.57 a

23.5 a

9.2 a

Quercetin -3rutinoside (mg kg-1) 1.5 a

b

20 40

75.2 aA 76.2 bA

65.6 aA 65.6 aA

5.2 aA 5.0 aA

31.9 aA 31.7 aA

18.0 aA 18.6 bA

5.9 aA 5.8 aA

0.14 bA 0.10 cA

0.57 aA 0.55 aA

21.2 bA 16.3 cA

8.9 aA 8.3 bA

1.5 aA 2.4 bA

60

77.3 cA

62.7 b

4.9 aA

30.0 bA

19.2 cA

4.9 bA

0.07 dA

0.53 bA

16.3 cA

8.4 bA

3.3 cA

80 100 20 40

77.9 78.8 82.0 78.2

61.4 60.6 63.4 62.4

4.7 4.5 4.4 4.0

29.2 28.0 31.3 30.1

19.8 19.5 17.9 18.5

4.7 4.4 5.6 4.8

0.06 0.06 0.13 0.08

0.50 0.49 0.53 0.45

16.3 16.7 14.8 16.9

7.2 6.6 4.3 6.9

4.3 2.9 2.2 2.5

60 80 20

73.1 dB 67.5 eB 78.4 bC

53.4 cB 51.1 dB 61.1 bC

3.5 dB 3.0 eB 4.2 bB

28.1 cB 26.4 dB 30.8 bB

18.1 aB 17.1 bB 16.5 bB

4.1 cB 3.5 dB 4.9 bB

0.06 dA 0.05 eA 0.08 bB

0.40 dB 0.31 eB 0.45 bC

11.2 dB 9.0 eB 11.5 bC

5.3 dB 3.8 bB 1.9 bA

1.5 aB 0.7 cB 4.1 bC

40

58.2 cC

54.6 cC

3.2 cC

25.9 cC

14.1 cB

3.0 cC

0.04 cB

0.28 cC

6.9 cB

1.6 bC

0.3 cB

cA d bB cB

cA cA bB bB

bA b bB cB

bA c aA bB

aA a aA aA

bA c aA bB

dA d bA cA

cA c bB cB

cA c bB cA

cA d bB cB

dA b bB bA

TP (mg kg−1 GAE) 857 a 863 aC 1069 cB 1199 dA 982 bA 835 a 925 aB 1163 cA 876 aB 744 bB 1092 bA 710 cC

Data are the mean of three replicates, each containing 30 fruits. ‘a’ means within the same temperature followed by different small letters are significantly different (LSD test, P < 0.05). ‘b’ means within the same days followed by different capital letters are significantly different (LSD test, P < 0.05). SSC means Soluble solids content. TA means Total acid. TP means Total phenolics.

3.3.1. Effect of the NFTS on antioxidant enzyme The activities of SOD, CAT, APX and GR exhibited the similar trend (Fig. 2A, B, C and D). The activities of these enzymes at all temperatures decreased with the increasing storage, which were negatively correlated with storage time (r was from 0.699 to 0.835, P ≤ 0.01) (Table 2). In comparison with 0 °C and 5 °C storage, NFTS showed slight fluctuation and maintained significantly (P < 0.05) higher activities of SOD, CAT, APX and GR. The activities of these enzymes in NFTS changes not significantly. The ROS, as the byproducts of various metabolic pathways, are continuously produced in different plants cellular compartment (Apel and Hirt, 2004). Generally the excess ROS could cause oxidative damage to cells which ultimately induced fruit senescence (Xia et al., 2016). Fortunately, plants possess the effective enzymatic antioxidant defense systems, including SOD, CAT, APX and GR, could scavenge ROS to safeguard plant cells from oxidative damage, which has been reported to be apart of the mechanism implicated in alleviation of lipid peroxidation and delay of senescence in many horticultural crops (Gao et al., 2016). Moreover, analysis of correlation indicated SOD and CAT had a positive correlation (r = 0.727, P ≤ 0.01) (Table 2). During storage life, SOD protected cells from oxidant stress by dismutating O2% to H2O2, and then CAT would be switched H2O2 to water. Besides, APX and GR are also able to convert hydrogen superoxide into water. Thus, high levels of antioxidant enzymes are critical to alleviate oxidative damage. Additionally, SOD and GR are correlated with maintenance of fruit quality in raspberry fruit (Harakotr et al., 2014). In our study, sweet cherry fruit stored at NFT had higher activities of antioxidative enzymes, which indicated that the degree of oxidative stress might be less serious in NFTS fruit.

displayed lower as compared with 0 °C and 5 °C storage. Moreover, the NFT inhibited the PPO activity more strictly and the changes were not significant during whole storage life. The results revealed a positive correlation between POD and PPO activities (r = 0.994, P ≤ 0.01) (Table 2). The inhibitory effect of NFTS on POD and PPO activities might attribute to a low respiration and biological metabolism. On the other hand, NFTS fruit displayed remarkably lower activity in both POD and PPO, probably as a result of alleviated fruit physiological disorder, usually occurring in traditional low temperature storage. Moreover, the higher content of ascorbic acid and phenolic compounds might inhibit POD and PPO activities (Denoya et al., 2012; Jang and Moon, 2011). The increase of LOX activity, owning to dioxygenation of polyunsaturated fatty acids causing toxic hydroperoxy fatty acids and membrane damage (Shewfelt and Rosario, 2000), was observed continuously increasing at all temperatures during the storage life (Fig. 2G). However, NFTS fruit displayed significantly (P < 0.05) lower LOX activity than 0 °C and 5 °C storage in the entire storage period, implying greater preservation of membrane integrity. The lipid hydroperoxides are formed and spontaneously decomposed to initiate a chain reaction of peroxidation of lipid by the oxy-free radicals (Gao et al., 2016). The lower LOX activity in NFTS sweet cherry fruit indicated the NFTS could be a novel method to prevent fruit oxidative damage for long time storage. 3.4. Effect of the NFTS on total soluble protein content Protein level was low in sweet cherry (Sharma et al., 2010). Protein content, from 0 °C and 5 °C groups, showed the slight increase in the initial stage, following by decrease during storage (Fig. 2H). We inferred that the increase of soluble protein might be attributed to hydrolysis of cell membrane induced by ripening (Scandalios, 1993), and ROS damage or fungal infection could cause the decrease trend of soluble protein in the fruit (Alia-Tejacal et al., 2007). But the NFT storage inhibited the loss and improved the level of protein in sweet cherries, which might indicate the NFTS could enhance resistance and membrane preservation of fruit.

3.3.2. Effect of the NFTS on POD, PPO and LOX activity Oxidation of phenolic compounds mediated by POD and PPO is another senescent symptom in fruit (Tomás-Barberán and Espín, 2010). For example, POD catalyses single electron oxidation of diverse antioxidant compounds and decomposes H2O2 in ROS scavenging. The present study exhibited the activities of POD and PPO with similar metabolic changes, and all temperatures storage displayed the continuously increasing trend (Fig. 2E and F). However, both the activities 117

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Fig. 2. Effect of the NFTS on SOD (A), CAT (B), APX (C), GR (D), POD (E), PPO (F), LOX (G) and activities and protein concentration (H) of ‘Tietonn’ sweet cherry fruit. Data are expressed as the mean ± SE (n = 3). Vertical bars represent the standard errors of the means.

3.5. NFTS alleviated the ion leakage raise and the production of MDA, H2O2 and O2%−

Moreover, MDA, H2O2 and O2%− had significantly positive correlation with POD, PPO and LOX (P ≤ 0.01) and negative correlation with SOD, APX and CAT (P ≤ 0.05). Ion leakage and MDA content are ordinarily considered as the indicators of membrane integrity and damage. Loss of membrane integrity under senescence stress during storage of fruit is generally linked with excessive of ROS including H2O2 and O2•¯ and the increasing of MDA and LOX level (Yang et al., 2014). Moreover, previous study suggested that the activated enzymatic antioxidant system contributed to ROS scavenging, inhibition of lipid peroxidation and peach fruit senescence (Flores et al., 2008). Additionally, the ascorbic acid content was negatively correlated with H2O2 content (r = 0.937, P ≤ 0.001) and O2%− production rate (r = 0.911, P ≤ 0.001) (Table 2), which was attributed to antioxidative enzymes could use ascorbate and H2O2 to produce water and dehydroascorbate (Tareen et al., 2012). Therefore, the reduced accumulation of MDA and ROS in sweet cherry fruit stored at NFT indicated that NFTS could provide protection from oxidative damage under senescence stress.

As shown in Fig. 3A and B, ion leakage increased rapidly before 40 d at 0 °C and 5 °C, while the MDA content increased gradually with storage increasing at all temperatures. The results observed that the ion leakage and MDA content at NFT fruit were 25.6% and 61.8% lower, respectively, than those at 0 °C and 5 °C in the end of storage. Furthermore, H2O2 coontent and O2%− production rate exhibited the similar trend with the change of ion leakage and MDA (Fig. 3C and D). The H2O2 production in NFTS fruit was about 55.6% lower than fruit stored at 0 °C in the end of storage, and the changes in NFTS group was not significant. Similarly, O2%− production rate of fruit increased gradually at 0 °C and 5 °C with storage time increasing, but NFTS obviously inhibited the rate increasing and maintained the initial level at the end of storage. As shown in Table 2, ion leakage was positively correlated with MDA (r = 0.965, P ≤ 0.01), H2O2 (r = 0.951, P ≤ 0.01), O2•¯ (r = 0.921, P ≤ 0.01) and LOX activity (r = 0.979, P ≤ 0.01). 118

119

1.000 －0.909** －0.308 0.357 －0.972** －0.979** －0.937** －0.911** 0.601*

0.790**

0.895**

0.452

－0.930** －0.937** －0.930** 0.413 0.350 －0.909** 0.301 －0.605* －0.442

CAT

1.000 0.606* －0.965** －0.916** －0.909** 0.308 0.273 －0.874** 0.238 －0.288 －0.699*

Ascorbic acid Carotenoid Anthocyanins TP Ion leakage MDA H2O2 O2•¯ SOD

APX

CAT

GR

PPO POD LOX DPPH FRAP L-TAA H-TAA Storage time Storage temperature

Traits

Ascorbic acid Carotenoid Anthocyanins TP Ion leakage MDA H2O2 O2•¯ SOD APX CAT GR PPO POD LOX DPPH FRAP L-TAA H-TAA Storage time Storage temperature 1.000 －0.585* －0.504 －0.497 0.532 0.711** －0.606* 0.658* 0.246 －0.730**

GR

0.937** 0.993** 0.986** －0.315 －0.238 0.909** －0.189 0.481 0.687*

－0.497

－0.923**

－0.748**

1.000 0.287 －0.238 0.972** 0.916** 0.937** 0.907** －0.566

Carotenoid

1.000 0.944** 0.958** －0.427 －0.357 0.867** －0.329 0.392 0.672*

PPO

0.301 0.252 0.259 0.084 0.413 －0.189 0.888** 0.384 0.079

0.249

－0.329

－0.189

1.000 0.469 0.287 0.336 0.295 0.270 0.028

Anthocyanins

1.000 0.993** －0.371 －0.301 0.930** －0.245 0.534 0.484

POD

－0.364 －0.294 －0.301 0.839** 0.923** －0.406 0.993** －0.121 －0.223

0.644*

0.273

0.427

1.000 －0.301 －0.392 －0.295 －0.361 0.524

TP

Correlation levels significant at * P < 0.05 and ** P < 0.01, respectively. (TP means total phenolics).

Ascorbic acid

Traits

1.000 －0.392 －0.308 0.902** －0.259 0.520 0.521

LOX

Table 2 Spearman’s correlation among antioxidant characters of sweet cherry fruits stored at 5 °C, 0 °C and NFT.

1.000 0.895** －0.469 0.832** －0.349 －0.144

DPPH

0.944** 0.986** 0.979** －0.378 －0.322 0.944** －0.252 0.541 0.495

－0.515

－0.916**

－0.804**

1.000 0.965** 0.951** 0.921** －0.629*

Ion leakage

1.000 －0.427 0.937** 0.096 －0.272

FRAP

0.951** 0.944** 0.937** －0.483 －0.399 0.923** －0.336 0.577* 0.480

1.000 0.944** 0.932** － 0.629* － 0.832** － 0.909** －0.518

MDA

1.000 －0.357 0.495 0.431

L-TAA

1.000 0.988** － 0.716** － 0.825** － 0.989** － 0.589* 0.968** 0.944** 0.933** －0.333 －0.305 0.912** －0.256 0.380 0.637*

H2O2

1.000 －0.043 －0.261

H-TAA

0.949** 0.914** 0.897** －0.371 －0.361 0.921** －0.322 0.321 0.655*

1.000 － 0.764** － 0.851** － 0.984** －0.644*

O2•¯

1.000 －0.396

Storage time

－0.699* －0.580* －0.587* 0.448 －0.594* －0.699* 0.545 0.171 － 0.835**

0.893**

0.727**

0.867**

1.000

SOD

1.000

Storage temperature

－0.860** －0.762** －0.776** 0.392 0.455 －0.776** 0.413 －0.096 －0.797**

－0.732**

0.825**

1.000

APX

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Fig. 3. Ion leakage (A), MDA content (B), H2O2 production (C) and O2%− production (D) changes of ‘Tieton’ sweet cherry fruit during cold storage at 5 °C, 0 °C and NFT. Data are expressed as the mean ± SE (n = 3). Vertical bars represent the standard errors of the means.

3.6. NFTS improved the antioxidant properties of sweet cherry fruit

antioxidant capacity than those of the 0 °C and 5 °C storage and roughly maintained the initial antioxidant ability. Additionally, the TP content was positively correlated with DPPH (r = 0.839, P ≤ 0.01) and FRAP (r = 0.923, P ≤ 0.01) (Table 2), thus the phenolic compounds were considered to be the mainly contribution to non-enzymatic antioxidant capacity. Other study showed the lower temperature storage could slightly increase antioxidant property at the end of the storage duration

The evolution of non-enzymatic antioxidants was showed in Fig. 4. DPPH radical scavenging activity and FRAP assay of flesh sweet cherry exhibited the similar pattern during the storage, showing an initial increase to the peak values, followed by decrease (Fig. 4A and B). At the end of storage, the NFTS fruit kept considerably higher levels of

Fig. 4. Effect of the NFTS on antioxidant activity and color change of ‘Tietonn’ sweet cherry fruit. DPPH scavenging (A), FRAP (B), lipophilic total antioxidant activities (L-TAA) (C), hydrophilic total antioxidant activities (H-TAA) (D). Data are expressed as the mean ± SE (n = 3). Vertical bars represent the standard errors of the means.

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in small fruits (Piljac-Žegarac and Šamec, 2011). The results indicated the NFTS could improve antioxidant potential of sweet cherry. TAA was measured in L-TAA and H-TAA fractions separately to research the antioxidant capacity of different fruit extracts. The results showed that H-TAA was 5-9-fold higher than L-TAA. The L-TAA increased in all temperatures storage, but the NFTS delayed and inhibited its accumulation. This pattern had a positive correlation with total carotenoids (r = 0.909, P ≤ 0.01) (Table 2), which indicated carotenoids could be the main lipophilic compounds with antioxidant activity in sweet cherry. In addition, H-TAA exhibited an initial increase, followed by a decrease during storage, and NFTS delayed the peak until 60 d and maintained the higher value at the end of storage. The H-TAA change had a positive correlation with anthocyanins (r = 0.888, P ≤ 0.01) and TP (r = 0.993, P ≤ 0.01), which was agreement with previous study, although ascorbic acid was also contributed to H-TAA (Usenik et al., 2008; Serrano et al., 2005). Generally, the ROS accumulation could cause oxidative damage to cell lipids, DNA and protein. Fortunately, antioxidant substances could block the harmful action of ROS, which scavenge free radicals and detoxify the organism (Wang et al., 2015a,b). Our results indicated that NFTS could improve the storability and health-promoting compounds of sweet cherry fruit by enhancing antioxidant activity.

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