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Effects of postharvest pulsed light treatments on the quality and antioxidant properties of persimmons during storage
Postharvest Biology and Technology 160 (2020) 111055
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Effects of postharvest pulsed light treatments on the quality and antioxidant properties of persimmons during storage
T
Gabriela I. Denoyaa,b,*, Gianpiero Pataroc,**, Giovanna Ferraric,d a
Instituto Nacional de Tecnología Agropecuaria (INTA), Instituto Tecnología de Alimentos, Buenos Aires, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina c Department of Industrial Engineering, University of Salerno, Via Giovanni Paolo II, 132, 84084 Fisciano SA Italy d ProdAl scarl, University of Salerno (Italy), Via Giovanni Paolo II, 132, 84084 Fisciano SA, Italy b
A R T I C LE I N FO
A B S T R A C T
Keywords: Persimmons Pulsed light Color Total phenols Vitamin C Antioxidant capacity
Pulsed light (PL) treatment for food consists in the application of a polychromatic light (wavelength: 200–1100 nm) in the form of intense but short pulses, frequently investigated as a decontamination method. In this work, the effects of PL treatments on the physicochemical properties, total phenolic content, vitamin C, and antioxidant capacity of persimmons (Diospyros kaki L. cv. Vanilla) at two different maturity stages (unripe yellow-green and ripe orange-red) during postharvest storage were investigated. The fruit were exposed to PL treatments at a dose of 20 kJ m−2 and 60 kJ m−2. Untreated and treated samples were allowed to ripe in dark conditions at 15 ± 1 °C for up to 6 d. The effects of PL treatments on the color, total soluble solids (TSS) as well as on total phenolic content, vitamin C and antioxidant capacity by three different methods were evaluated during storage and compared with those of untreated samples. Results showed that the physicochemical properties (color and TSS) and vitamin C content of the fruit were not affected by the PL treatments over the storage period. On the other hand, the total phenols content and the antioxidant capacity were significantly (p < 0.05) affected by the treatments. Considering that these parameters were related to the soluble tannins in persimmons and these compounds are related to the astringency of these fruit, this work encourages the research of the potential application of PL as a de-astringency method for persimmons.
1. Introduction
tannins, which, therefore, provide the major contribution to the overall antioxidant capacity of persimmon fruit (Del Bubba et al., 2009; Homnava et al., 1990). The antioxidant capacity of several varieties was also investigated using different methods, such as 2,2-diphenyl-1picrylhydrazyl (DPPH), 2,2´- azinobis (3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) and superoxide radicals, highlighting the notable antioxidant properties of these fruit (Del Bubba et al., 2009). It is well known that the content of bioactive compounds with antioxidant and antimicrobial activity in climacteric fruit, such as persimmons, may vary greatly depending not only on the variety, cultivation methods and environmental factors (such as nutrient availability, temperature and light) but mostly on the postharvest handling practices (Jagadeesh et al., 2011). Therefore, in recent years, many works were focused on the development of effective and sustainable postharvest methods not only to extend the shelf life but also to preserve or even to increase the content of antioxidant compounds of
Persimmons (Diospyros kaki L.) are climacteric fruit with unique sensory characteristics and nutritional quality. As for many other commodities, the external color of persimmons is the property used as a non-destructive index for harvesting. During ripening, the color of the persimmon epidermis varies from green at the immature stage to a bright red when the fruit is at the last stages of ripeness (Salvador et al., 2007). Persimmons are a good source of biologically active compounds such as ascorbic acid, tannins and carotenoids, which are related to many physiological functions including a protective role against oxidative stress-related diseases, and anti-mutagenic and anti-carcinogenic capacities. Several works have investigated the content of different antioxidant compounds in various persimmon cultivars, demonstrating that carotenoids are present at lower concentrations than vitamin C and
⁎
Corresponding author at: Instituto Tecnología de Alimentos, Instituto Nacional de Tecnología Agropecuaria (INTA), CC 25 – CP 1712, Castelar, Buenos Aires, Argentina. ⁎⁎ Corresponding author. E-mail addresses: [email protected] (G.I. Denoya), [email protected] (G. Pataro). https://doi.org/10.1016/j.postharvbio.2019.111055 Received 17 April 2019; Received in revised form 23 August 2019; Accepted 24 October 2019 0925-5214/ © 2019 Elsevier B.V. All rights reserved.
Postharvest Biology and Technology 160 (2020) 111055
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lamp housing and is equipped with an adjustable 0.16 x 0.41 m stainless steel tray which allows changing the vertical distance from the lamp source from 0.08 to 0.22 m. The ozone and heat generated both at the housing lamp and at the treatment zone are removed by a forced-air system with filter. The persimmons of the two maturity stages (unripe and ripe) were divided into three groups of fifteen units each. One group of fruit from unripe and one from ripe maturity stage were used as control while one group from each maturity stage was exposed to a PL treatment of 20 kJ m−2 and the other group was exposed to a PL treatment of 60 kJ m−2. In order to guarantee the treatment uniformity and to reduce the effect of the heat generated by the pulsed light emission, the samples were disposed in the middle of the chamber and aligned with their axis parallel to the lamp tube at the maximum vertical distance allowed (0.22 m). As per the manufacturer specifications, at this distance, the fluence delivered per each pulse on the upper surface of the sample was 5.7 kJ m−2. The persimmons of each group were exposed to the desired energy dose on one side and then, rotated 180° and exposed to the same dose at the other side. The total doses applied per each side were 20 and 60 kJ m−2 and were achieved using exposure times per each side of 1.2 and 3.5 s, respectively. Then, the treatments evaluated were:
fruit and vegetables (Pataro et al., 2015a; Ribeiro et al., 2012). This would contribute to reduce food losses and to enhance the market value of fresh produce with high nutritional and health beneficial properties Particularly, it has been demonstrated that the postharvest exposure of many fruit and vegetables to Pulsed Light (PL) may cause stress in plant tissues, which stimulates the biosynthesis of defensive secondary metabolites with antimicrobial and antioxidant activity (Pataro et al., 2015a; Aguiló-Aguayo et al., 2017; Luksiene et al., 2012; Ribeiro et al., 2012). The PL treatments consist in the exposure of fresh produce to a polychromatic light (200–1100 nm) including ultraviolet (180–400 nm), visible (400–700 nm) and near-infrared (700–1100 nm) wavelengths in the form of intense but short pulses (1 μs – 0.1 s) emitted by an inert gas (e.g. xenon) lamp (Oms-Oliu, Martin-Belloso & SolivaFortuny, 2010). It is important to highlight that the short exposure times of PL treatments could significantly promote the utilization of this technology at the industrial scale (Pataro et al., 2015a). Nevertheless, while the potential use of PL technology for food decontamination has been extensively investigated (Cacace and Palmieri, 2014; Gómez-López, 2016; Oms-Oliu et al., 2010; Mahendran et al., 2019), only very few studies have been carried out to investigate the potential applications of PL as a postharvest treatment to improve the nutritional quality or to enhance the content of antioxidant compounds and the effects of the treatments on the physicochemical properties of fruit and vegetables. For instance, Koyyalamudi et al. (2011) have reported that PL treatment (range: 2 kJ m−2 to 100 kJ m−2) provides a highly effective way for increasing Vitamin D2 content in button mushrooms (Agaricus bisporus). On the other hand, the photoactivation of anthocyanin production has been successfully used to enhance the color of apples (Dong et al., 1995). Besides, Rodov et al. (2012) reported an increase in the total anthocyanin and phenolic compounds content in figs. Murugesan et al. (2012) reported that PL enhanced the antioxidant properties of elderberry fruit by increasing their total polyphenolic content. Aguiló-Aguayo et al. (2017) observed a slight increase in the carotenoids concentrations in carrots slices and Aguiló-Aguayo et al. (2013), in whole tomatoes. Moreover, Pataro et al. (2015a) reported an increase of the biosynthesis of antioxidant compounds in tomatoes without modifying their physicochemical properties by appliying PL and, in another work, an increase of total phenols in Annurca apple fruit (Pataro et al., 2015b). However, to the best of our knowledge, there are no publications dealing with the evaluation of the effects of PL on persimmon fruit. Then, the aim of this study was to evaluate the effects of postharvest PL treatments on the color, soluble solids, total phenols content and antioxidant capacity of persimmon at two different maturation stages during storage.
1) 0 kJ m−2 Control (without treatment): for Unripe and Ripe fruit 2) 20 kJ m−2 (Time of exposure = 1.2 s, Frequency 3 s-1, 5.7 kJ m−2 per pulse): for Unripe and Ripe fruit 3) 60 kJ m−2 (Time of exposure = 3.5 s, Frequency 3 s-1, 5.7 kJ m−2 per pulse): for Unripe and Ripe fruit The PL treatments were carried out starting with the samples at room temperature (20 ± 2 °C). The maximum temperature increase on the surface of the samples was not greater than 2 °C. The fruit of each group were placed, without contact between each other, in aluminum trays (three trays with five fruit each) and then stored under dark conditions for up to 6 d at 15 ± 2 °C. At specified times (0, 3, and 6 d), one tray with five fruit from each treatment was randomly chosen for carrying out the following determinations: color parameters, total soluble solids, vitamin C, total phenols and antioxidant capacity by three different methods. The explanation of the different methods is explained hereunder. 2.3. Color parameters Color parameters of the persimmons were measured with a CR400 Chroma Meter (Konika Minolta Inc., Japan) using the CIE L* a* b* scale where L* represents lightness, a* (red to green color) and b* (yellow to blue color). The equipment was set up for illuminant D65 and 2° observer angle and calibrated using a standard white tile. Each measurement was taken randomly at three points per sample of fruit.
2. Materials and methods 2.1. Plant material Persimmon (Diospyros kaki L. cv. Vanilla) fruit were harvested in the province of Salerno (southern Italy) in autumn 2018 at two different stages of maturity: I-yellow-green (unripe) and II-orange-red (ripe) (Fig. 1). After harvesting, the fruit were transported to the laboratory and, on the same day, treated with PL. Fruit of uniform (almost spherical) shape and size (approximately 8 cm in diameter) were selected and the ones damaged and of poor quality were discarded.
2.4. Physicochemical and biochemical analyses At each specified storage time, the pericarp from the equatorial region of five persimmon fruit of each lot was excised and cut into small pieces using a sharp knife. All steps of these determinations were carried in ground ice, to avoid sample oxidation. The pieces were then combined, and about 40 g were homogenized in a laboratory blender (Sterilmixer 12, International PBI S.p.A., Milano, Italy) operated at medium speed (key 4) for 1 min. Aliquots of the homogenized sample were used for the physicochemical and biochemical analyses described in the following sections.
2.2. Pulsed light treatments PL treatments of persimmons were carried out in a bench-top RS3000 C SteriPulse XL system (Xenon Corp., Wilmington, Mass., USA), described in detail by Pataro et al. (2015a). Briefly, it comprises a power/control module, a treatment chamber and a lamp housing with a linear 16″ xenon flash lamp. The system generates three pulses per second (360 μs width) of polychromatic light in the wavelength range between 200 and 1100 nm. The treatment chamber is placed below the
2.5. Total soluble solids (TSS) The soluble solid content was determined on the supernatant recovered after the centrifugation of each homogenized sample by 2
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Fig. 1. Pictures of (a) unripe and (b) ripe persimmons (Diospyros kaki L. cv. Vanilla).
2.6.3.2. DPPH method. The ability of the extracts to neutralize the 2,2Diphenyl-1-picrylhydrazyl (DPPH) free radicals was determined by the method described by Ribeiro et al. (2008). Thirty microliters of the extract prepared in 2.6.2 and diluted conveniently were mixed with 200 μL of a 0.1 mM DPPH (Sigma Aldrich, Milan, Italy) methanolic solution. The mix was vortexed and was allowed to react for 30 min in the dark at room temperature (25 °C). Subsequently, the absorbance at 517 nm was measured. The results were expressed as grams of gallic acid equivalents (GAE) per kilogram of fresh weight: g kg−1 (GAE).
measuring the refraction index with an Abbe digital refractometer model DR-A1 (ATAGO CO., LTD, USA) at 25 °C and expressed as a percentage (%). 2.6. Total Phenols and antioxidant capacity 2.6.1. Extraction for Total Phenols and antioxidant capacity The extraction for total phenols and antioxidant capacity determinations was carried out according to Denoya et al. (2017). Two grams of the homogenized samples were mixed with 2 mL of aqueous methanol (80%, v/v). Afterward, the samples were vortexed for 2 min and centrifuged at 10,000 x g for 10 min at 4 °C. The supernatant obtained from each sample was used to carry out the following determinations.
2.6.3.3. Ferric reducing antioxidant power (FRAP) method. The FRAP method measures the reduction potential of the antioxidants present in the samples and in this work it was assessed according to the method described by Müller et al. (2010). Briefly, 50 μL of the extract prepared in 2.6.1 and diluted conveniently, were mixed with 200 μL of the FRAP reactive (prepared at the moment of the determination in this way: solution 10:10:1 300 mmol L−1 of acetate buffer (pH 3.6): 20 mmol L−1 FeCl3 : 10 mmol L−1 2,4,6-Tris(2-pyridyl)-s-triazine (TPTZ) (SigmaAldrich, Steinheim, Germany) in 40 mmol L−1 HCl. The ferric [Fe (III)] TPTZ compound formed was reduced at its form Fe (II) by the antioxidants. After 30 min of incubation at room temperature (25 °C), the absorbance of the samples at 593 nm was measured with a MR-96A Microplate Reader (Shenzhen Mindray Bio-Medical Electronics Co., Ltd, China). The results were expressed as grams of equivalents of Trolox per kilogram of fresh fruit (g kg−1 eq Trolox).
2.6.2. Total phenols determination The total phenol determination was carried out according to Singleton et al. (1999), adapted for its realization in microplate wells. A volume of 20 μL of the supernatant from each sample obtained at 2.6.1 was mixed with 100 μL of Folin-Ciocalteau reagent (Sigma Aldrich, Milan, Italy) in a microplate well. The mix was vortexed and was allowed to react for 2 min. Then, 180 μL of a saturated Na2CO3 (Sigma Aldrich, Milan, Italy) (aq.) solution (75 g L−1) was added to each well. After incubation at room temperature for 2 h, the absorbance of the reaction mixture was measured at 760 nm against a blank using a MR96A Microplate Reader (Shenzhen Mindray Bio-Medical Electronics Co., Ltd, China). The content of total phenols was calculated based on a calibration curve with gallic acid (G7384, Sigma Aldrich, Milan, Italy) and was expressed as grams of gallic acid equivalents (GAE) per kilogram. Results are expressed on a fresh weight (FW) basis.
2.7. Vitamin C For the vitamin C extraction, 2 g of fruit was mixed with 5 mL of buffer phosphate 0.2 M pH 2.14. Then, the mix was vortexed for 2 min and centrifuged at 10,000 x g for 10 min at 4 °C and the supernatant was used for the quantification of vitamin C by high-performance liquid chromatography (HPLC). Vitamin C was separated using a Waters 1525series HPLC system, equipped with a Waters 2996 photodiode array detector (DAD) (Waters Corporation, USA) and a Waters Spherisorb column (5um ODS2, 4.6 x 150 mm). The separation was carried out with a flow rate of 0.01 mL s−1 of buffer phosphate 0.2 M pH 2.14 as a mobile phase; the wavelength used for detection was 240 nm and the injection volume was 10 μL. A calibration curve was obtained from a stock solution prepared by dissolving vitamin C standard (BP461, Sigma Aldrich, Steinheim, Germany) in the buffer used as the mobile phase.
2.6.3. Antioxidant capacity 2.6.3.1. ABTS method. The antioxidant capacity by the ABTS method was determined spectrophotometrically at 734 nm with the 2,2´ - azinobis [3-ethylbenzothiazoline-6 sulfonicacid] diammonium salt (ABTS) reagent (Sigma-Aldrich, Steinheim, Germany), according to the technique reported by Rohn et al. (2004). This method is based on the scavenging of long-lived radical anions (ABTS•). The radicals are generated by mixing ABTS with potassium persulfate. Fifty microliters of the extract prepared in 2.6.1 and diluted conveniently were mixed with 200 μL of a 0.42 mM ABTS solution. After 6 min of incubation at room temperature, the absorbance of the mixture was measured at 734 nm by using a MR-96A Microplate Reader (Shenzhen Mindray BioMedical Electronics Co., Ltd, China). The antioxidant capacity was expressed in Trolox (6-hydroxy-2,5,7,8-tetramethylchroman-2carboxylic acid) equivalents (TEAC): mol kg−1 (eq. Trolox). Trolox was purchased from Acros Organics, Geel, Belgium. Results are expressed on a fresh weight basis.
2.8. Statistical analysis All the irradiation treatments and analyses were performed in duplicate unless otherwise stated, and the mean and standard error of the 3
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analysis was performed using the General Linear Model procedure from SAS (Version 9.2 2002e2003 SAS Institute Inc. Cary, NC, USA). Tukey's test (significance level of 0.05) was performed for the data presented in tables and graphics. 3. Results and discussion 3.1. Color parameters Fig. 2 shows the changes in L*, a*, and b* parameters for unripe and ripe persimmon fruit subjected to the different PL treatments and during storage at 15 °C. The darkening of the fruit (expressed as a decrease in L* value) (Fig. 2a) and the development of red coloration (expressed as an increase in a* value) (Fig. 2b) were the major trends in the fruit color changes during storage. In the case of the PL-treated unripe fruit, the shift in a* parameter from negative to positive values reflected the change in their color from light-green to red. Generally, just after the treatments the L* value was significantly lower (p < 0.05) for the ripe fruit in comparison to the unripe fruit but there were no differences between the fruit subjected to the different PL treatments, with the exception of the ripe fruit subjected to 60 kJ m−2 in which the L* value was similar to that of the unripe fruit. After three days of storage, the ripe fruit treated with PL were significantly (p < 0.05) darker (lower values of L*) than all the unripe fruit and the ones treated with 60 kJ m-2 were also darker (p < 0.05) than the control ripe fruit. At 6 d of storage at 15 °C, there were no significant differences in the L* values of all the samples analyzed from all the treatments. The L* value decreased during storage for all the samples. Although any comparison with data found in current literature is very difficult due to the different types of equipment, species, cultivars and experimental conditions used, our results appear to be consistent with those reported in previous works. For example, a similar darkening effect (lower L* value) was observed by Khademi et al. (2013) in persimmons exposed to UV-C light (1.5 kJ m−2 and 3 kJ m−2) after three days of storage in comparison with untreated fruit. Rodov et al. (2012) reported that a PL treatment of 2 kJ m−2 was enough to develop darkening in poorly colored ‘Brown Turkey’ figs. In that work, PL effects were already evident even 1 d after treatment and the phenomenon was fully expressed after 5 d of storage. According to these authors, the exposure to PL might stimulate higher production of photoprotective anthocyanins induced in plant tissues under stressful conditions, in order to alleviate the damage caused by high radiation. In our work it also seems that the effects of PL on L* parameter, need at least three days to take place since immediately after treatment at 60 kJm−2, the samples were not darker but even lighter than the control samples. In the case of a* parameter (Fig. 2b), there was a significant difference between ripe and unripe fruit after the first and the third day of storage, but there were no differences (p > 0.05) in the values between control and treated samples and among the values of all the samples at the last day of analysis. The a* value increased during storage for all the unripe samples. Imaizumi et al. (2018) also reported an increase of a* parameter and a decrease of L* parameter on persimmons during storage. However, in contrast with our findings, they observed a blackening on the persimmon surfaces irradiated with UV light (12.9 W m−2 up to 15 min), which was related to the transfer of tannins from the parenchyma tissue to the epidermal tissue. On the other hand, when Sanchís et al. (2015) processed fresh-cut persimmons and evaluated them during refrigerated storage, they related the decrease in L* and the increase in a* parameters to enzymatic browning. In the case of b* parameter (Fig. 2c), the trend was similar than the one for L* parameter. Just after the treatments, the b* value was significantly lower (p < 0.05) for the ripe fruit in comparison to the unripe fruit, but no differences were detected between the fruit subjected to the different PL treatments, with the exception of the ripe fruit subjected to 60 kJ m−2 in which b* value was similar to that measured for the unripe fruit.
Fig. 2. Means values for color parameters: L* (brightness) (A), a* (red to green color) (B), and b* (yellow to blue color) (C) of untreated (0 kJ m−2) and PL treated unripe and ripe persimmons during storage at 15 °C. Values with different lowercase letters within the same day of analysis are significantly different (p < 0.05), while values with different uppercase letters within the same PL dose are significantly different (p < 0.05) according to Tukey´s test. Vertical bars represent standard error (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article).
experimental values were calculated. Differences among mean values were analyzed by means of the one-way analysis of variance (ANOVA) in order to determine whether different light treatment and storage period led to a significant difference in the physicochemical properties as well as antioxidant compounds content of persimmons. Statistical 4
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Table 1 . Total soluble solids (%) in untreated (0 kJ m−2) and PL treated persimmons during storage at 15 °C. Maturity stage
Dose kJ m−2
Table 2 Total phenolic content in untreated (0 kJ m−2) and PL treated persimmons during storage at 15 °C.
Total soluble solids (%)
Maturity stage
Dose kJ m−2
Total phenols g kg−1 (Gallic Acid eq.)
Days of storage at 15 °C Days of storage at 15 °C 0
3
6 0
Unripe
Ripe
0 20 60 0 20 60
13.1 15.4 15.1 13.7 15.6 14.9
+ + + + + +
0.2 0.1 0.1 0.4 0.1 0.1
aA aA aA aA aA aA
15.3 14.7 14.2 14.2 15.6 16.4
+ + + + + +
0.2 0.1 0.3 0.2 0.1 0.1
aA aB aA aA aA aA
13.9 14.4 14.8 14.2 15.2 18.3
+ + + + + +
0.2 0.1 0.1 0.2 0.7 0.1
aA aB aA aA aA aA
Unripe
Ripe
Values with different lowercase letters within the same column are significantly different (p < 0.05), while values with different uppercase letters within the same row are significantly different (p < 0.05) according to Tukey´s test. Data are expressed as means + Std. Error.
0 20 60 0 20 60
0.3 5.0 3.9 1.0 1.5 0.6
3 + + + + + +
0.1 0.1 0.5 0.1 0.3 0.1
bB aA abA abA abA bA
6.5 1.4 3.3 0.7 0.4 0.3
6 + + + + + +
0.3 0.1 0.8 0.1 0.1 0.1
aA bB abA bA bA bA
0.7 1.2 1.2 0.6 0.5 0.5
+ + + + + +
0.1 0.3 0.1 0.1 0.1 0.1
aB aB aA aA aA aA
Values with different lowercase letters within the same column are significantly different (p < 0.05), while values with different uppercase letters within the same row are significantly different (p < 0.05) according to Tukey´s test. Data are expressed as means + Std. Error.
After three days of storage, the b* values measured for ripe fruit exposed to 20 and 60 kJ m−2 were significantly (p < 0.05) lower than the ones measured for all the unripe samples and control ripe fruit. Moreover, regardless of the maturity stage, after 6 d of storage no significant (p > 0.05) differences could be observed between the different samples. Similarly, Rodov et al. (2012) also observed a significant reduction in the b* parameter after PL treatments on figs indicating the fading of the yellowish tint.
in the total phenolic content between the persimmons subjected to the different treatments. In addition, after three days of storage, the control samples of unripe fruit presented a higher amount of total phenols in comparison to the first day of analysis and the value was also higher than all the other samples analyzed that day. It seems that in unripe fruit, there was a peak in the concentration of phenols that was produced in the PL treated samples before that is was produced in the control ones. Besides, it should be noticed that, in persimmons, the total phenols content is mainly related to soluble tannins (Giordani et al., 2011), whose concentration during the first period of fruit development typically exhibited a significant increase, which could be related to the synthesis of proanthocyanidins (Del Bubba et al., 2009). Then, when fruit ripening proceeds, the concentration of soluble tannins tends to decrease, in agreement with our results of Table 2. If the fruit is left to ripen on the tree, this decline in soluble tannin concentration could be due to the increment of the fruit weight, and in overripe fruit, the decrease is accelerated probably due to the transformation of soluble tannins into their insoluble form. It is important to highlight that, although after six days of storage there were no significant differences (p < 0.05) between the total phenols content in all the samples, the concentration of these compounds in the fruit treated with 60 kJ m−2 was the most stable during the period analyzed.
3.2. Total soluble solids Table 1 shows the results obtained for the total soluble solids measured as % for unripe and ripe persimmons subjected to the different PL treatments. Immediately after the treatments and after 3 d and 6 d of storage, although the persimmons treated with PL have a slightly higher amount of soluble solids than the untreated samples, the values were not statistically significant (p > 0.05). This is in agreement with Besada et al. (2009) that reported that the soluble solids content of persimmons harvested at different maturations stages were not significantly different. On the other hand, in the case of unripe fruit and for the treatment at 20 kJ m−2, there was a significant decrease in soluble solids during storage. This reduction could be possibly due to the condensation of soluble tannins in the form of insoluble compounds as it happens after the application of some de-astringency methods (Öz et al., 2004). The changes in soluble solids are usually related to the ripening of fruit (Luo, 2006) and according to Salvador et al. (2007), the measurement of total soluble solids also includes the soluble tannins, which are related to astringency in these fruit. Therefore, the decrease observed after PL treatment could be due to the reduction of soluble tannins and the consequent formation of insoluble compounds, which are non-astringents (Arnal and Del Río, 2003). However, further investigations are necessary to confirm this hypothesis.
3.4. Antioxidant capacity Table 3 shows the results obtained for antioxidant capacity by a) ABTS, b) DPPH and c) FRAP methods of unripe and ripe persimmons subjected to the different PL treatment. The trend for antioxidant capacity evaluated by the three methods is the same for all the samples and similar to the one observed for total phenols (Table 2). This is in agreement with Chen et al. (2008) that reported a positive and highly significant correlation between the content of total phenols and radical scavenging activity against ABTS and DPPH radicals in persimmons, suggesting that persimmons have similar ability to scavenge the radicals evaluated. Leong and Shui (2002) also observed similar trends for these determinations on other fruit and vegetables. Thus, in the case of unripe persimmons and for all the methods (ABTS, DPPH, and FRAP), the fruit treated with PL presented a higher antioxidant capacity than the control ones just after the treatments, and this difference is statistically significant (p < 0.05) for the samples measured by ABTS and FRAP method. According to Solovchenko and Merzlyak (2008), this could be due to a photo-protective antioxidant defense response to oxidative stress caused by the light treatments. Pataro et al. (2015a) also reported that PL treatments were effective in activating biosynthesis pathways of compounds with high antioxidant potential in green tomatoes. Similarly, Liu et al. (2012) observed a
3.3. Total phenols Table 2 shows the results obtained for total phenols of unripe and ripe persimmons subjected to the different PL treatments and during storage at 15 °C. In the case of the unripe persimmons, the total phenol content of the fruit exposed to 20 kJ m−2 presented a statistically significant (p < 0.05) higher concentration of total phenols than the control ones just after the treatment. This is in agreement with AguilóAguayo et al. (2013) and Rodov et al. (2012) that observed an antioxidant defense response to oxidative stress in fruit after PL treatments. Moreover, Murugesan et al. (2012) reported that pulsed UV light treatments (11 kJ m−2) enhanced the antioxidant properties of elderberry fruit by increasing their total polyphenolic content. However, in the case of ripe fruit, there were no significant (p > 0.05) differences 5
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the PL treatments. This was in agreement with Aguiló-Aguayo et al. (2013) that reported that PL treatments of 26.8 kJ m-2 and 53.6 kJ m-2 did not affect the content of vitamin C in tomatoes and with Luksiene et al. (2012) that observed the same in different fruit and vegetables exposed at 54 kJ m-2 PL treatment.
Table 3 Antioxidant capacity by a) ABTS method b) FRAP method and c)DPPH method of untreated (0 kJ m−2) and PL treated persimmons during storage at 15 °C. Maturity stage
Dose (kJ m−2)
Antioxidant capacity mol kg−1 (eq Trolox) Days of storage at 15 °C
Unripe
Ripe
Maturity stage
0 20 60 0 20 60 Dose kJ m−2
0
3
6
2 + 1 bB 27 + 1 a A 21 + 3 ab A 5+1bA 7 + 3 ab A 3+1bA
33 + 1 a A 3+1bB 14 + 4 ab A 4+1bA 3+1bA 2+1bA
3 5 5 2 2 2
4. Conclusions + + + + + +
1 1 1 1 1 1
a a a a a a
1 2 1 1 1 1
aB aB aA aA aA aA
The results of this study have demonstrated that regardless of the maturity stage, postharvest PL treatments assayed in this work (20 kJ m−2 and 60 kJ m−2) did not affect the physicochemical parameters analyzed of persimmons. On the other hand, there was an effect on soluble solids, total phenols and antioxidant capacity of the treatments on unripe fruit. This could be possibly related to an effect on the soluble tannins content of persimmons. Considering that these compounds are related to the astringency in this fruit, further studies should be done including other determinations (e.g. sensory analysis, acetaldehyde production, soluble and insoluble tannins) to investigate if PL treatments could be used as a de-astringency method. We consider that this is an interesting research topic to evaluate the postharvest commercial application of this technology.
B B A A A A
Antioxidant capacity mol kg−1 (eq Trolox) Days of storage at 15 °C
Unripe
Ripe
Maturity stage
0 20 60 0 20 60 Dose kJ m−2
0
3
6
1 + 1 bB 37 + 1 aA 28 + 4 abA 6 + 1 abA 9 + 2 abA 3 + 1 bA
43 + 1 aA 2 + 1 bB 18 + 6 abA 4 + 1 abA 2 + 1 bA 1 + 1 bA
4 7 8 2 2 2
+ + + + + +
Acknowledgments The authors greatly acknowledge Roberta Ferrari for her help in the management of Dr. Denoya´s Research stay at ProdAl, Fisciano, Italy and Mariangela Falcone for her technical assistance in the chemical determinations.
Antioxidant capacity g kg−1 (Gallic Acid eq) Days of storage at 15 °C 0
Unripe
Ripe
0 20 60 0 20 60
0.1 0.9 0.8 0.3 0.4 0.1
3 + + + + + +
0.1 0.1 0.1 0.1 0.2 0.1
aA aA aA aA aA aA
0.6 0.1 0.5 0.2 0.1 0.1
6 + + + + + +
0.1 0.1 0.2 0.1 0.1 0.1
aA aA aA aA aA aA
0.2 0.4 0.4 0.1 0.1 0.1
+ + + + + +
0.1 0.1 0.1 0.1 0.1 0.1
References
aA aA aA aA aA aA
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Values with different lowercase letters within the same column are significantly different (p < 0.05), while values with different uppercase letters within the same row are significantly different (p < 0.05) according to Tukey´s test. Data are expressed as means + Std. Error.
higher accumulation of total phenolics, flavonoids, as well as a greater antioxidant capacity in tomato fruit exposed to either 4 or 8 kJ m−2 UVC doses in comparison to the ones observed in untreated samples. However, in the case of ripe persimmons, the differences between the treatments were not significantly different. In addition, after three days of storage, the control unripe fruit presented a higher antioxidant capacity in comparison to the first day of analysis and this value was also higher than the ones of all the other samples analyzed that day. It seems that in unripe fruit, the same maximum observed in total phenols (Table 2) was also observed for antioxidant capacity and that was produced before in the PL treated samples. After six days of storage, the values for antioxidant capacity were significantly lower (p < 0.05) for all the samples and the values were not significantly different between the treatments. This decrease during storage could be explained mainly by the insolubilization process of soluble tannins but also by the polymerization process of proanthocyanidins (Del Bubba et al., 2009). Although there is an important decrease of antioxidant capacity during storage, it is important to highlight that regardless the variety, the antioxidant capacity is much higher in persimmons than the one observed for other fruit (e.g. apples) (Lamperi et al., 2008), thus confirming the antioxidant properties of these fruit. 3.5. Vitamin C The vitamin C content was in the range of 0.1 g kg−1 - 0.2 g kg−1 fruit (FW) in all the samples (data not shown) and was not affected by 6
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Öz, A.T., Özelkök, I.S., Albayrak, B., 2004. Sugar and tannin content changes in persimmon fruit during artificial ripening with dry ice. V Int. Postharvest Symp. 682, 987–992. Pataro, G., Sinik, M., Capitoli, M.M., Donsì, G., Ferrari, G., 2015a. The influence of postharvest UV-C and pulsed light treatments on quality and antioxidant properties of tomato fruits during storage. Innov. Food Sci. Emerg. Technol. 30, 103–111. Pataro, G., Donsì, G., Ferrari, G., 2015b. Post-harvest UV-C and PL irradiation of fruits and vegetables. Chem. Eng. Res. Des. 44, 31–36. Ribeiro, S.M.R., Barbosa, L.C.A., Queiroz, J.H., Knödler, M., Schieber, A., 2008. Phenolic compounds and antioxidant capacity of Brazilian mango (Mangifera indica L.) varieties. Food Chem. 110, 620–626. Ribeiro, C., Canada, J., Alvarenga, B., 2012. Prospects of UV radiation for application in postharvest technology. Emir. J. Food Agric. 24, 586–597. Rodov, V., Vinokur, Y., Horev, B., 2012. Brief postharvest exposure to pulsed light stimulates coloration and anthocyanin accumulation in fig fruit (Ficus carica L.). Postharvest Biol. Technol. 68, 43–46. Rohn, S., Rawel, H.M., Kroll, J., 2004. Antioxidant activity of protein-bound quercetin. J. Agric. Food Chem. 52, 4725–4729. Salvador, A., Arnal, L., Besada, C., Larrea, V., Quiles, A., Pérez-Munuera, I., 2007. Physiological and structural changes during ripening and deastringency treatment of persimmon fruit cv. ‘Rojo Brillante’. Postharvest Biol. Technol. 46, 181–188. Sanchís, E., Mateos, M., Pérez-Gago, M.B., 2015. Effect of maturity stage at processing and antioxidant treatments on the physico-chemical, sensory and nutritional quality of fresh-cut ‘Rojo Brillante’ persimmon. Postharvest Biol. Technol. 105, 34–44. Singleton, V.L., Orthofer, R., Lamuela-Raventós, R.M., 1999. Analysis of Total Phenols and Other Oxidation Substrates and Antioxidants by Means of Folin-ciocalteu Reagent, Methods in Enzymology. Academic Press, pp. 152–178. Solovchenko, A.E., Merzlyak, M.N., 2008. Screening of visible and UV radiation as a photoprotective mechanism in plants. Russ. J. Plant Physiol. 55, 719.
storage at cold temperature. Int. Food Res. J. 20, 247–253. Koyyalamudi, S.R., Jeong, S.-C., Pang, G., Teal, A., Biggs, T., 2011. Concentration of vitamin D2 in white button mushrooms (Agaricus bisporus) exposed to pulsed UV light. J. Food Compos. Anal. 24, 976–979. Lamperi, L., Chiuminatto, U., Cincinelli, A., Galvan, P., Giordani, E., Lepri, L., Del Bubba, M., 2008. Polyphenol levels and free radical scavenging activities of four apple cultivars from integrated and organic farming in different italian areas. J. Agric. Food Chem. 56, 6536–6546. Leong, L.P., Shui, G., 2002. An investigation of antioxidant capacity of fruits in Singapore markets. Food Chem. 76, 69–75. Liu, C.-h., Cai, L.-y., Lu, X.-y., Han, X.-x., Ying, T.-j., 2012. Effect of postharvest UV-C irradiation on phenolic compound content and antioxidant activity of tomato fruit during storage. J. Integr. Agric. 11, 159–165. Luksiene, Z., Buchovec, I., Kairyte, K., Paskeviciute, E., Viskelis, P., 2012. High-power pulsed light for microbial decontamination of some fruits and vegetables with different surfaces. J. Food Agric. Environ. 10, 162–167. Luo, Z., 2006. Extending shelf-life of persimmon (Diospyros kaki L.) fruit by hot air treatment. Eur. Food Res. Technol. 222, 149–154. Mahendran, R., Ramanan, K.R., Barba, F.J., Lorenzo, J.M., López-Fernández, O., Munekata, P.E.S., Roohinejad, S., Sant’Ana, A.S., Tiwari, B.K., 2019. Recent advances in the application of pulsed light processing for improving food safety and increasing shelf life. Trends Food Sci. Technol. 88, 67–79. Müller, L., Gnoyke, S., Popken, A.M., Böhm, V., 2010. Antioxidant capacity and related parameters of different fruit formulations. Lwt - Food Sci. Technol. 43, 992–999. Murugesan, R., Orsat, V., Lefsrud, M., 2012. Effect of pulsed ultraviolet light on the total phenol content of elderberry (Sambucus nigra) fruit. Food Nutr. Sci. 3, 774. Oms-Oliu, G., Aguiló-Aguayo, I., Martín-Belloso, O., Soliva-Fortuny, R., 2010. Effects of pulsed light treatments on quality and antioxidant properties of fresh-cut mushrooms (Agaricus bisporus). Postharvest Biol. Technol. 56, 216–222.
7
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Postharvest Biology and Technology journal homepage: www.elsevier.com/locate/postharvbio
Effects of postharvest pulsed light treatments on the quality and antioxidant properties of persimmons during storage
T
Gabriela I. Denoyaa,b,*, Gianpiero Pataroc,**, Giovanna Ferraric,d a
Instituto Nacional de Tecnología Agropecuaria (INTA), Instituto Tecnología de Alimentos, Buenos Aires, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina c Department of Industrial Engineering, University of Salerno, Via Giovanni Paolo II, 132, 84084 Fisciano SA Italy d ProdAl scarl, University of Salerno (Italy), Via Giovanni Paolo II, 132, 84084 Fisciano SA, Italy b
A R T I C LE I N FO
A B S T R A C T
Keywords: Persimmons Pulsed light Color Total phenols Vitamin C Antioxidant capacity
Pulsed light (PL) treatment for food consists in the application of a polychromatic light (wavelength: 200–1100 nm) in the form of intense but short pulses, frequently investigated as a decontamination method. In this work, the effects of PL treatments on the physicochemical properties, total phenolic content, vitamin C, and antioxidant capacity of persimmons (Diospyros kaki L. cv. Vanilla) at two different maturity stages (unripe yellow-green and ripe orange-red) during postharvest storage were investigated. The fruit were exposed to PL treatments at a dose of 20 kJ m−2 and 60 kJ m−2. Untreated and treated samples were allowed to ripe in dark conditions at 15 ± 1 °C for up to 6 d. The effects of PL treatments on the color, total soluble solids (TSS) as well as on total phenolic content, vitamin C and antioxidant capacity by three different methods were evaluated during storage and compared with those of untreated samples. Results showed that the physicochemical properties (color and TSS) and vitamin C content of the fruit were not affected by the PL treatments over the storage period. On the other hand, the total phenols content and the antioxidant capacity were significantly (p < 0.05) affected by the treatments. Considering that these parameters were related to the soluble tannins in persimmons and these compounds are related to the astringency of these fruit, this work encourages the research of the potential application of PL as a de-astringency method for persimmons.
1. Introduction
tannins, which, therefore, provide the major contribution to the overall antioxidant capacity of persimmon fruit (Del Bubba et al., 2009; Homnava et al., 1990). The antioxidant capacity of several varieties was also investigated using different methods, such as 2,2-diphenyl-1picrylhydrazyl (DPPH), 2,2´- azinobis (3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) and superoxide radicals, highlighting the notable antioxidant properties of these fruit (Del Bubba et al., 2009). It is well known that the content of bioactive compounds with antioxidant and antimicrobial activity in climacteric fruit, such as persimmons, may vary greatly depending not only on the variety, cultivation methods and environmental factors (such as nutrient availability, temperature and light) but mostly on the postharvest handling practices (Jagadeesh et al., 2011). Therefore, in recent years, many works were focused on the development of effective and sustainable postharvest methods not only to extend the shelf life but also to preserve or even to increase the content of antioxidant compounds of
Persimmons (Diospyros kaki L.) are climacteric fruit with unique sensory characteristics and nutritional quality. As for many other commodities, the external color of persimmons is the property used as a non-destructive index for harvesting. During ripening, the color of the persimmon epidermis varies from green at the immature stage to a bright red when the fruit is at the last stages of ripeness (Salvador et al., 2007). Persimmons are a good source of biologically active compounds such as ascorbic acid, tannins and carotenoids, which are related to many physiological functions including a protective role against oxidative stress-related diseases, and anti-mutagenic and anti-carcinogenic capacities. Several works have investigated the content of different antioxidant compounds in various persimmon cultivars, demonstrating that carotenoids are present at lower concentrations than vitamin C and
⁎
Corresponding author at: Instituto Tecnología de Alimentos, Instituto Nacional de Tecnología Agropecuaria (INTA), CC 25 – CP 1712, Castelar, Buenos Aires, Argentina. ⁎⁎ Corresponding author. E-mail addresses: [email protected] (G.I. Denoya), [email protected] (G. Pataro). https://doi.org/10.1016/j.postharvbio.2019.111055 Received 17 April 2019; Received in revised form 23 August 2019; Accepted 24 October 2019 0925-5214/ © 2019 Elsevier B.V. All rights reserved.
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lamp housing and is equipped with an adjustable 0.16 x 0.41 m stainless steel tray which allows changing the vertical distance from the lamp source from 0.08 to 0.22 m. The ozone and heat generated both at the housing lamp and at the treatment zone are removed by a forced-air system with filter. The persimmons of the two maturity stages (unripe and ripe) were divided into three groups of fifteen units each. One group of fruit from unripe and one from ripe maturity stage were used as control while one group from each maturity stage was exposed to a PL treatment of 20 kJ m−2 and the other group was exposed to a PL treatment of 60 kJ m−2. In order to guarantee the treatment uniformity and to reduce the effect of the heat generated by the pulsed light emission, the samples were disposed in the middle of the chamber and aligned with their axis parallel to the lamp tube at the maximum vertical distance allowed (0.22 m). As per the manufacturer specifications, at this distance, the fluence delivered per each pulse on the upper surface of the sample was 5.7 kJ m−2. The persimmons of each group were exposed to the desired energy dose on one side and then, rotated 180° and exposed to the same dose at the other side. The total doses applied per each side were 20 and 60 kJ m−2 and were achieved using exposure times per each side of 1.2 and 3.5 s, respectively. Then, the treatments evaluated were:
fruit and vegetables (Pataro et al., 2015a; Ribeiro et al., 2012). This would contribute to reduce food losses and to enhance the market value of fresh produce with high nutritional and health beneficial properties Particularly, it has been demonstrated that the postharvest exposure of many fruit and vegetables to Pulsed Light (PL) may cause stress in plant tissues, which stimulates the biosynthesis of defensive secondary metabolites with antimicrobial and antioxidant activity (Pataro et al., 2015a; Aguiló-Aguayo et al., 2017; Luksiene et al., 2012; Ribeiro et al., 2012). The PL treatments consist in the exposure of fresh produce to a polychromatic light (200–1100 nm) including ultraviolet (180–400 nm), visible (400–700 nm) and near-infrared (700–1100 nm) wavelengths in the form of intense but short pulses (1 μs – 0.1 s) emitted by an inert gas (e.g. xenon) lamp (Oms-Oliu, Martin-Belloso & SolivaFortuny, 2010). It is important to highlight that the short exposure times of PL treatments could significantly promote the utilization of this technology at the industrial scale (Pataro et al., 2015a). Nevertheless, while the potential use of PL technology for food decontamination has been extensively investigated (Cacace and Palmieri, 2014; Gómez-López, 2016; Oms-Oliu et al., 2010; Mahendran et al., 2019), only very few studies have been carried out to investigate the potential applications of PL as a postharvest treatment to improve the nutritional quality or to enhance the content of antioxidant compounds and the effects of the treatments on the physicochemical properties of fruit and vegetables. For instance, Koyyalamudi et al. (2011) have reported that PL treatment (range: 2 kJ m−2 to 100 kJ m−2) provides a highly effective way for increasing Vitamin D2 content in button mushrooms (Agaricus bisporus). On the other hand, the photoactivation of anthocyanin production has been successfully used to enhance the color of apples (Dong et al., 1995). Besides, Rodov et al. (2012) reported an increase in the total anthocyanin and phenolic compounds content in figs. Murugesan et al. (2012) reported that PL enhanced the antioxidant properties of elderberry fruit by increasing their total polyphenolic content. Aguiló-Aguayo et al. (2017) observed a slight increase in the carotenoids concentrations in carrots slices and Aguiló-Aguayo et al. (2013), in whole tomatoes. Moreover, Pataro et al. (2015a) reported an increase of the biosynthesis of antioxidant compounds in tomatoes without modifying their physicochemical properties by appliying PL and, in another work, an increase of total phenols in Annurca apple fruit (Pataro et al., 2015b). However, to the best of our knowledge, there are no publications dealing with the evaluation of the effects of PL on persimmon fruit. Then, the aim of this study was to evaluate the effects of postharvest PL treatments on the color, soluble solids, total phenols content and antioxidant capacity of persimmon at two different maturation stages during storage.
1) 0 kJ m−2 Control (without treatment): for Unripe and Ripe fruit 2) 20 kJ m−2 (Time of exposure = 1.2 s, Frequency 3 s-1, 5.7 kJ m−2 per pulse): for Unripe and Ripe fruit 3) 60 kJ m−2 (Time of exposure = 3.5 s, Frequency 3 s-1, 5.7 kJ m−2 per pulse): for Unripe and Ripe fruit The PL treatments were carried out starting with the samples at room temperature (20 ± 2 °C). The maximum temperature increase on the surface of the samples was not greater than 2 °C. The fruit of each group were placed, without contact between each other, in aluminum trays (three trays with five fruit each) and then stored under dark conditions for up to 6 d at 15 ± 2 °C. At specified times (0, 3, and 6 d), one tray with five fruit from each treatment was randomly chosen for carrying out the following determinations: color parameters, total soluble solids, vitamin C, total phenols and antioxidant capacity by three different methods. The explanation of the different methods is explained hereunder. 2.3. Color parameters Color parameters of the persimmons were measured with a CR400 Chroma Meter (Konika Minolta Inc., Japan) using the CIE L* a* b* scale where L* represents lightness, a* (red to green color) and b* (yellow to blue color). The equipment was set up for illuminant D65 and 2° observer angle and calibrated using a standard white tile. Each measurement was taken randomly at three points per sample of fruit.
2. Materials and methods 2.1. Plant material Persimmon (Diospyros kaki L. cv. Vanilla) fruit were harvested in the province of Salerno (southern Italy) in autumn 2018 at two different stages of maturity: I-yellow-green (unripe) and II-orange-red (ripe) (Fig. 1). After harvesting, the fruit were transported to the laboratory and, on the same day, treated with PL. Fruit of uniform (almost spherical) shape and size (approximately 8 cm in diameter) were selected and the ones damaged and of poor quality were discarded.
2.4. Physicochemical and biochemical analyses At each specified storage time, the pericarp from the equatorial region of five persimmon fruit of each lot was excised and cut into small pieces using a sharp knife. All steps of these determinations were carried in ground ice, to avoid sample oxidation. The pieces were then combined, and about 40 g were homogenized in a laboratory blender (Sterilmixer 12, International PBI S.p.A., Milano, Italy) operated at medium speed (key 4) for 1 min. Aliquots of the homogenized sample were used for the physicochemical and biochemical analyses described in the following sections.
2.2. Pulsed light treatments PL treatments of persimmons were carried out in a bench-top RS3000 C SteriPulse XL system (Xenon Corp., Wilmington, Mass., USA), described in detail by Pataro et al. (2015a). Briefly, it comprises a power/control module, a treatment chamber and a lamp housing with a linear 16″ xenon flash lamp. The system generates three pulses per second (360 μs width) of polychromatic light in the wavelength range between 200 and 1100 nm. The treatment chamber is placed below the
2.5. Total soluble solids (TSS) The soluble solid content was determined on the supernatant recovered after the centrifugation of each homogenized sample by 2
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Fig. 1. Pictures of (a) unripe and (b) ripe persimmons (Diospyros kaki L. cv. Vanilla).
2.6.3.2. DPPH method. The ability of the extracts to neutralize the 2,2Diphenyl-1-picrylhydrazyl (DPPH) free radicals was determined by the method described by Ribeiro et al. (2008). Thirty microliters of the extract prepared in 2.6.2 and diluted conveniently were mixed with 200 μL of a 0.1 mM DPPH (Sigma Aldrich, Milan, Italy) methanolic solution. The mix was vortexed and was allowed to react for 30 min in the dark at room temperature (25 °C). Subsequently, the absorbance at 517 nm was measured. The results were expressed as grams of gallic acid equivalents (GAE) per kilogram of fresh weight: g kg−1 (GAE).
measuring the refraction index with an Abbe digital refractometer model DR-A1 (ATAGO CO., LTD, USA) at 25 °C and expressed as a percentage (%). 2.6. Total Phenols and antioxidant capacity 2.6.1. Extraction for Total Phenols and antioxidant capacity The extraction for total phenols and antioxidant capacity determinations was carried out according to Denoya et al. (2017). Two grams of the homogenized samples were mixed with 2 mL of aqueous methanol (80%, v/v). Afterward, the samples were vortexed for 2 min and centrifuged at 10,000 x g for 10 min at 4 °C. The supernatant obtained from each sample was used to carry out the following determinations.
2.6.3.3. Ferric reducing antioxidant power (FRAP) method. The FRAP method measures the reduction potential of the antioxidants present in the samples and in this work it was assessed according to the method described by Müller et al. (2010). Briefly, 50 μL of the extract prepared in 2.6.1 and diluted conveniently, were mixed with 200 μL of the FRAP reactive (prepared at the moment of the determination in this way: solution 10:10:1 300 mmol L−1 of acetate buffer (pH 3.6): 20 mmol L−1 FeCl3 : 10 mmol L−1 2,4,6-Tris(2-pyridyl)-s-triazine (TPTZ) (SigmaAldrich, Steinheim, Germany) in 40 mmol L−1 HCl. The ferric [Fe (III)] TPTZ compound formed was reduced at its form Fe (II) by the antioxidants. After 30 min of incubation at room temperature (25 °C), the absorbance of the samples at 593 nm was measured with a MR-96A Microplate Reader (Shenzhen Mindray Bio-Medical Electronics Co., Ltd, China). The results were expressed as grams of equivalents of Trolox per kilogram of fresh fruit (g kg−1 eq Trolox).
2.6.2. Total phenols determination The total phenol determination was carried out according to Singleton et al. (1999), adapted for its realization in microplate wells. A volume of 20 μL of the supernatant from each sample obtained at 2.6.1 was mixed with 100 μL of Folin-Ciocalteau reagent (Sigma Aldrich, Milan, Italy) in a microplate well. The mix was vortexed and was allowed to react for 2 min. Then, 180 μL of a saturated Na2CO3 (Sigma Aldrich, Milan, Italy) (aq.) solution (75 g L−1) was added to each well. After incubation at room temperature for 2 h, the absorbance of the reaction mixture was measured at 760 nm against a blank using a MR96A Microplate Reader (Shenzhen Mindray Bio-Medical Electronics Co., Ltd, China). The content of total phenols was calculated based on a calibration curve with gallic acid (G7384, Sigma Aldrich, Milan, Italy) and was expressed as grams of gallic acid equivalents (GAE) per kilogram. Results are expressed on a fresh weight (FW) basis.
2.7. Vitamin C For the vitamin C extraction, 2 g of fruit was mixed with 5 mL of buffer phosphate 0.2 M pH 2.14. Then, the mix was vortexed for 2 min and centrifuged at 10,000 x g for 10 min at 4 °C and the supernatant was used for the quantification of vitamin C by high-performance liquid chromatography (HPLC). Vitamin C was separated using a Waters 1525series HPLC system, equipped with a Waters 2996 photodiode array detector (DAD) (Waters Corporation, USA) and a Waters Spherisorb column (5um ODS2, 4.6 x 150 mm). The separation was carried out with a flow rate of 0.01 mL s−1 of buffer phosphate 0.2 M pH 2.14 as a mobile phase; the wavelength used for detection was 240 nm and the injection volume was 10 μL. A calibration curve was obtained from a stock solution prepared by dissolving vitamin C standard (BP461, Sigma Aldrich, Steinheim, Germany) in the buffer used as the mobile phase.
2.6.3. Antioxidant capacity 2.6.3.1. ABTS method. The antioxidant capacity by the ABTS method was determined spectrophotometrically at 734 nm with the 2,2´ - azinobis [3-ethylbenzothiazoline-6 sulfonicacid] diammonium salt (ABTS) reagent (Sigma-Aldrich, Steinheim, Germany), according to the technique reported by Rohn et al. (2004). This method is based on the scavenging of long-lived radical anions (ABTS•). The radicals are generated by mixing ABTS with potassium persulfate. Fifty microliters of the extract prepared in 2.6.1 and diluted conveniently were mixed with 200 μL of a 0.42 mM ABTS solution. After 6 min of incubation at room temperature, the absorbance of the mixture was measured at 734 nm by using a MR-96A Microplate Reader (Shenzhen Mindray BioMedical Electronics Co., Ltd, China). The antioxidant capacity was expressed in Trolox (6-hydroxy-2,5,7,8-tetramethylchroman-2carboxylic acid) equivalents (TEAC): mol kg−1 (eq. Trolox). Trolox was purchased from Acros Organics, Geel, Belgium. Results are expressed on a fresh weight basis.
2.8. Statistical analysis All the irradiation treatments and analyses were performed in duplicate unless otherwise stated, and the mean and standard error of the 3
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analysis was performed using the General Linear Model procedure from SAS (Version 9.2 2002e2003 SAS Institute Inc. Cary, NC, USA). Tukey's test (significance level of 0.05) was performed for the data presented in tables and graphics. 3. Results and discussion 3.1. Color parameters Fig. 2 shows the changes in L*, a*, and b* parameters for unripe and ripe persimmon fruit subjected to the different PL treatments and during storage at 15 °C. The darkening of the fruit (expressed as a decrease in L* value) (Fig. 2a) and the development of red coloration (expressed as an increase in a* value) (Fig. 2b) were the major trends in the fruit color changes during storage. In the case of the PL-treated unripe fruit, the shift in a* parameter from negative to positive values reflected the change in their color from light-green to red. Generally, just after the treatments the L* value was significantly lower (p < 0.05) for the ripe fruit in comparison to the unripe fruit but there were no differences between the fruit subjected to the different PL treatments, with the exception of the ripe fruit subjected to 60 kJ m−2 in which the L* value was similar to that of the unripe fruit. After three days of storage, the ripe fruit treated with PL were significantly (p < 0.05) darker (lower values of L*) than all the unripe fruit and the ones treated with 60 kJ m-2 were also darker (p < 0.05) than the control ripe fruit. At 6 d of storage at 15 °C, there were no significant differences in the L* values of all the samples analyzed from all the treatments. The L* value decreased during storage for all the samples. Although any comparison with data found in current literature is very difficult due to the different types of equipment, species, cultivars and experimental conditions used, our results appear to be consistent with those reported in previous works. For example, a similar darkening effect (lower L* value) was observed by Khademi et al. (2013) in persimmons exposed to UV-C light (1.5 kJ m−2 and 3 kJ m−2) after three days of storage in comparison with untreated fruit. Rodov et al. (2012) reported that a PL treatment of 2 kJ m−2 was enough to develop darkening in poorly colored ‘Brown Turkey’ figs. In that work, PL effects were already evident even 1 d after treatment and the phenomenon was fully expressed after 5 d of storage. According to these authors, the exposure to PL might stimulate higher production of photoprotective anthocyanins induced in plant tissues under stressful conditions, in order to alleviate the damage caused by high radiation. In our work it also seems that the effects of PL on L* parameter, need at least three days to take place since immediately after treatment at 60 kJm−2, the samples were not darker but even lighter than the control samples. In the case of a* parameter (Fig. 2b), there was a significant difference between ripe and unripe fruit after the first and the third day of storage, but there were no differences (p > 0.05) in the values between control and treated samples and among the values of all the samples at the last day of analysis. The a* value increased during storage for all the unripe samples. Imaizumi et al. (2018) also reported an increase of a* parameter and a decrease of L* parameter on persimmons during storage. However, in contrast with our findings, they observed a blackening on the persimmon surfaces irradiated with UV light (12.9 W m−2 up to 15 min), which was related to the transfer of tannins from the parenchyma tissue to the epidermal tissue. On the other hand, when Sanchís et al. (2015) processed fresh-cut persimmons and evaluated them during refrigerated storage, they related the decrease in L* and the increase in a* parameters to enzymatic browning. In the case of b* parameter (Fig. 2c), the trend was similar than the one for L* parameter. Just after the treatments, the b* value was significantly lower (p < 0.05) for the ripe fruit in comparison to the unripe fruit, but no differences were detected between the fruit subjected to the different PL treatments, with the exception of the ripe fruit subjected to 60 kJ m−2 in which b* value was similar to that measured for the unripe fruit.
Fig. 2. Means values for color parameters: L* (brightness) (A), a* (red to green color) (B), and b* (yellow to blue color) (C) of untreated (0 kJ m−2) and PL treated unripe and ripe persimmons during storage at 15 °C. Values with different lowercase letters within the same day of analysis are significantly different (p < 0.05), while values with different uppercase letters within the same PL dose are significantly different (p < 0.05) according to Tukey´s test. Vertical bars represent standard error (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article).
experimental values were calculated. Differences among mean values were analyzed by means of the one-way analysis of variance (ANOVA) in order to determine whether different light treatment and storage period led to a significant difference in the physicochemical properties as well as antioxidant compounds content of persimmons. Statistical 4
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Table 1 . Total soluble solids (%) in untreated (0 kJ m−2) and PL treated persimmons during storage at 15 °C. Maturity stage
Dose kJ m−2
Table 2 Total phenolic content in untreated (0 kJ m−2) and PL treated persimmons during storage at 15 °C.
Total soluble solids (%)
Maturity stage
Dose kJ m−2
Total phenols g kg−1 (Gallic Acid eq.)
Days of storage at 15 °C Days of storage at 15 °C 0
3
6 0
Unripe
Ripe
0 20 60 0 20 60
13.1 15.4 15.1 13.7 15.6 14.9
+ + + + + +
0.2 0.1 0.1 0.4 0.1 0.1
aA aA aA aA aA aA
15.3 14.7 14.2 14.2 15.6 16.4
+ + + + + +
0.2 0.1 0.3 0.2 0.1 0.1
aA aB aA aA aA aA
13.9 14.4 14.8 14.2 15.2 18.3
+ + + + + +
0.2 0.1 0.1 0.2 0.7 0.1
aA aB aA aA aA aA
Unripe
Ripe
Values with different lowercase letters within the same column are significantly different (p < 0.05), while values with different uppercase letters within the same row are significantly different (p < 0.05) according to Tukey´s test. Data are expressed as means + Std. Error.
0 20 60 0 20 60
0.3 5.0 3.9 1.0 1.5 0.6
3 + + + + + +
0.1 0.1 0.5 0.1 0.3 0.1
bB aA abA abA abA bA
6.5 1.4 3.3 0.7 0.4 0.3
6 + + + + + +
0.3 0.1 0.8 0.1 0.1 0.1
aA bB abA bA bA bA
0.7 1.2 1.2 0.6 0.5 0.5
+ + + + + +
0.1 0.3 0.1 0.1 0.1 0.1
aB aB aA aA aA aA
Values with different lowercase letters within the same column are significantly different (p < 0.05), while values with different uppercase letters within the same row are significantly different (p < 0.05) according to Tukey´s test. Data are expressed as means + Std. Error.
After three days of storage, the b* values measured for ripe fruit exposed to 20 and 60 kJ m−2 were significantly (p < 0.05) lower than the ones measured for all the unripe samples and control ripe fruit. Moreover, regardless of the maturity stage, after 6 d of storage no significant (p > 0.05) differences could be observed between the different samples. Similarly, Rodov et al. (2012) also observed a significant reduction in the b* parameter after PL treatments on figs indicating the fading of the yellowish tint.
in the total phenolic content between the persimmons subjected to the different treatments. In addition, after three days of storage, the control samples of unripe fruit presented a higher amount of total phenols in comparison to the first day of analysis and the value was also higher than all the other samples analyzed that day. It seems that in unripe fruit, there was a peak in the concentration of phenols that was produced in the PL treated samples before that is was produced in the control ones. Besides, it should be noticed that, in persimmons, the total phenols content is mainly related to soluble tannins (Giordani et al., 2011), whose concentration during the first period of fruit development typically exhibited a significant increase, which could be related to the synthesis of proanthocyanidins (Del Bubba et al., 2009). Then, when fruit ripening proceeds, the concentration of soluble tannins tends to decrease, in agreement with our results of Table 2. If the fruit is left to ripen on the tree, this decline in soluble tannin concentration could be due to the increment of the fruit weight, and in overripe fruit, the decrease is accelerated probably due to the transformation of soluble tannins into their insoluble form. It is important to highlight that, although after six days of storage there were no significant differences (p < 0.05) between the total phenols content in all the samples, the concentration of these compounds in the fruit treated with 60 kJ m−2 was the most stable during the period analyzed.
3.2. Total soluble solids Table 1 shows the results obtained for the total soluble solids measured as % for unripe and ripe persimmons subjected to the different PL treatments. Immediately after the treatments and after 3 d and 6 d of storage, although the persimmons treated with PL have a slightly higher amount of soluble solids than the untreated samples, the values were not statistically significant (p > 0.05). This is in agreement with Besada et al. (2009) that reported that the soluble solids content of persimmons harvested at different maturations stages were not significantly different. On the other hand, in the case of unripe fruit and for the treatment at 20 kJ m−2, there was a significant decrease in soluble solids during storage. This reduction could be possibly due to the condensation of soluble tannins in the form of insoluble compounds as it happens after the application of some de-astringency methods (Öz et al., 2004). The changes in soluble solids are usually related to the ripening of fruit (Luo, 2006) and according to Salvador et al. (2007), the measurement of total soluble solids also includes the soluble tannins, which are related to astringency in these fruit. Therefore, the decrease observed after PL treatment could be due to the reduction of soluble tannins and the consequent formation of insoluble compounds, which are non-astringents (Arnal and Del Río, 2003). However, further investigations are necessary to confirm this hypothesis.
3.4. Antioxidant capacity Table 3 shows the results obtained for antioxidant capacity by a) ABTS, b) DPPH and c) FRAP methods of unripe and ripe persimmons subjected to the different PL treatment. The trend for antioxidant capacity evaluated by the three methods is the same for all the samples and similar to the one observed for total phenols (Table 2). This is in agreement with Chen et al. (2008) that reported a positive and highly significant correlation between the content of total phenols and radical scavenging activity against ABTS and DPPH radicals in persimmons, suggesting that persimmons have similar ability to scavenge the radicals evaluated. Leong and Shui (2002) also observed similar trends for these determinations on other fruit and vegetables. Thus, in the case of unripe persimmons and for all the methods (ABTS, DPPH, and FRAP), the fruit treated with PL presented a higher antioxidant capacity than the control ones just after the treatments, and this difference is statistically significant (p < 0.05) for the samples measured by ABTS and FRAP method. According to Solovchenko and Merzlyak (2008), this could be due to a photo-protective antioxidant defense response to oxidative stress caused by the light treatments. Pataro et al. (2015a) also reported that PL treatments were effective in activating biosynthesis pathways of compounds with high antioxidant potential in green tomatoes. Similarly, Liu et al. (2012) observed a
3.3. Total phenols Table 2 shows the results obtained for total phenols of unripe and ripe persimmons subjected to the different PL treatments and during storage at 15 °C. In the case of the unripe persimmons, the total phenol content of the fruit exposed to 20 kJ m−2 presented a statistically significant (p < 0.05) higher concentration of total phenols than the control ones just after the treatment. This is in agreement with AguilóAguayo et al. (2013) and Rodov et al. (2012) that observed an antioxidant defense response to oxidative stress in fruit after PL treatments. Moreover, Murugesan et al. (2012) reported that pulsed UV light treatments (11 kJ m−2) enhanced the antioxidant properties of elderberry fruit by increasing their total polyphenolic content. However, in the case of ripe fruit, there were no significant (p > 0.05) differences 5
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the PL treatments. This was in agreement with Aguiló-Aguayo et al. (2013) that reported that PL treatments of 26.8 kJ m-2 and 53.6 kJ m-2 did not affect the content of vitamin C in tomatoes and with Luksiene et al. (2012) that observed the same in different fruit and vegetables exposed at 54 kJ m-2 PL treatment.
Table 3 Antioxidant capacity by a) ABTS method b) FRAP method and c)DPPH method of untreated (0 kJ m−2) and PL treated persimmons during storage at 15 °C. Maturity stage
Dose (kJ m−2)
Antioxidant capacity mol kg−1 (eq Trolox) Days of storage at 15 °C
Unripe
Ripe
Maturity stage
0 20 60 0 20 60 Dose kJ m−2
0
3
6
2 + 1 bB 27 + 1 a A 21 + 3 ab A 5+1bA 7 + 3 ab A 3+1bA
33 + 1 a A 3+1bB 14 + 4 ab A 4+1bA 3+1bA 2+1bA
3 5 5 2 2 2
4. Conclusions + + + + + +
1 1 1 1 1 1
a a a a a a
1 2 1 1 1 1
aB aB aA aA aA aA
The results of this study have demonstrated that regardless of the maturity stage, postharvest PL treatments assayed in this work (20 kJ m−2 and 60 kJ m−2) did not affect the physicochemical parameters analyzed of persimmons. On the other hand, there was an effect on soluble solids, total phenols and antioxidant capacity of the treatments on unripe fruit. This could be possibly related to an effect on the soluble tannins content of persimmons. Considering that these compounds are related to the astringency in this fruit, further studies should be done including other determinations (e.g. sensory analysis, acetaldehyde production, soluble and insoluble tannins) to investigate if PL treatments could be used as a de-astringency method. We consider that this is an interesting research topic to evaluate the postharvest commercial application of this technology.
B B A A A A
Antioxidant capacity mol kg−1 (eq Trolox) Days of storage at 15 °C
Unripe
Ripe
Maturity stage
0 20 60 0 20 60 Dose kJ m−2
0
3
6
1 + 1 bB 37 + 1 aA 28 + 4 abA 6 + 1 abA 9 + 2 abA 3 + 1 bA
43 + 1 aA 2 + 1 bB 18 + 6 abA 4 + 1 abA 2 + 1 bA 1 + 1 bA
4 7 8 2 2 2
+ + + + + +
Acknowledgments The authors greatly acknowledge Roberta Ferrari for her help in the management of Dr. Denoya´s Research stay at ProdAl, Fisciano, Italy and Mariangela Falcone for her technical assistance in the chemical determinations.
Antioxidant capacity g kg−1 (Gallic Acid eq) Days of storage at 15 °C 0
Unripe
Ripe
0 20 60 0 20 60
0.1 0.9 0.8 0.3 0.4 0.1
3 + + + + + +
0.1 0.1 0.1 0.1 0.2 0.1
aA aA aA aA aA aA
0.6 0.1 0.5 0.2 0.1 0.1
6 + + + + + +
0.1 0.1 0.2 0.1 0.1 0.1
aA aA aA aA aA aA
0.2 0.4 0.4 0.1 0.1 0.1
+ + + + + +
0.1 0.1 0.1 0.1 0.1 0.1
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aA aA aA aA aA aA
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higher accumulation of total phenolics, flavonoids, as well as a greater antioxidant capacity in tomato fruit exposed to either 4 or 8 kJ m−2 UVC doses in comparison to the ones observed in untreated samples. However, in the case of ripe persimmons, the differences between the treatments were not significantly different. In addition, after three days of storage, the control unripe fruit presented a higher antioxidant capacity in comparison to the first day of analysis and this value was also higher than the ones of all the other samples analyzed that day. It seems that in unripe fruit, the same maximum observed in total phenols (Table 2) was also observed for antioxidant capacity and that was produced before in the PL treated samples. After six days of storage, the values for antioxidant capacity were significantly lower (p < 0.05) for all the samples and the values were not significantly different between the treatments. This decrease during storage could be explained mainly by the insolubilization process of soluble tannins but also by the polymerization process of proanthocyanidins (Del Bubba et al., 2009). Although there is an important decrease of antioxidant capacity during storage, it is important to highlight that regardless the variety, the antioxidant capacity is much higher in persimmons than the one observed for other fruit (e.g. apples) (Lamperi et al., 2008), thus confirming the antioxidant properties of these fruit. 3.5. Vitamin C The vitamin C content was in the range of 0.1 g kg−1 - 0.2 g kg−1 fruit (FW) in all the samples (data not shown) and was not affected by 6
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