Impaginato 205 Adv. Hort. Sci., 2020 34(2): 205­212 DOI: 10.13128/ahsc­8255 Aloe vera coatings maintain antioxi­ dants of fig (Ficus carica L.) fruit during storage A. Mirshekari 1 (*), B. Madani 2, M. Wall 3, A.R. Biggs 4 1 Department of Agronomy and Plant Breeding, Yasouj University, Yasouj, Iran. 2 Horticultural Crops Research Department, Natural Resources Research and Education Center of Hormozgan, AREEO, Bandar Abbas, Iran. 3 U.S. Department of Agriculture, Agricultural Research Service, Hilo, HI, USA. 4 West Virginia University, Tree Fruit Research and Education Center, Kearneysville, WV, USA. Key words: coating, Ficus carica, phytochemicals, quality. Abstract: Demand for fig fruit is increasing because of its high antioxidant capacity and health benefit for human. So, interest in maintaining bioactive components of fruit has been increased. However, antioxidant capacity of fruits decreases during storage. Fresh fruits of the well­known fig (Ficus carica L.) cul­ tivar ‘Siyah’ were grown in Fars Province, Iran, treated with different concen­ trations of Aloe vera gel prior to being placed into cold storage. We examined fruit for firmness, soluble solids contents, anthocyanin concentrations, total phenolic compounds, flavonoid concentrations, ascorbic acid content, antioxi­ dant activity, phenylalanine ammonia­lyase and superoxide dismutase activi­ ties. Figs coated with Aloe vera gel maintained higher firmness, anthocyanin concentrations, total phenolic compounds, flavonoid concentrations, ascorbic acid content, and antioxidant capacity than the control. Phenylalanine ammo­ nia­lyase and superoxide dismutase activities were enhanced with Aloe vera gel treatments. The results showed that Aloe vera gel treatments could be an alter­ native to the current chemical protocols for preserving nutraceutical traits of fig fruit by maintaining antioxidant capacity during storage. 1. Introduction Fig fruit is an important part of the Mediterranean food and is rich in fibers and antioxidant compounds (Arvaniti et al., 2019). Antioxidant compounds are rich in fruits like fig and can prevent free radical forma­ tion. Foods which are rich in phytochemicals decrease incidence of dis­ ease and maintain body healthful (Singh, 2016). For this reason, it is important to use these phytochemicals in our diet (Singh, 2016). It has been detected that anthocyanin intake can prevent heart diseases and promote anti­carcinogenic and hypoglycemic activities. Thus, high con­ tent of anthocyanin has made fig attractive for consumers. Also, figs con­ (*) Corresponding author: a_mirshekari@yu.ac.ir Citation: MIRSHEKARI A., MADANI B., WALL M., BIGGS A.R., 2020 ­ Aloe vera coatings maintain antioxi‐ dants of fig (Ficus carica L.) fruit during storage. ‐ Adv. Hort. Sci., 34(2): 205­212. Copyright: © 2020 Mirshekari A., Madani B., Wall M., Biggs A.R. This is an open access, peer reviewed article published by Firenze University Press (http://www.fupress.net/index.php/ahs/) and distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Competing Interests: The authors declare no competing interests. Received for publication 16 May 2019 Accepted for publication 31 October 2019 AHS Advances in Horticultural Science http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ Adv. Hort. Sci., 2020 34(2): 205­212 206 tain high level of flavonoid which reduces oxidative stress (Reyes­Avalos et al., 2016). Delicate epidermal tissue, climacteric behavior and extensive softening make fig fruit susceptible to the wounding and spoilage which limit shelf life of fruit (Bahar and Lichter, 2018). Also, it has been confirmed that antioxidant activity of fruits decreases during storage (Madani et al., 2016). Therefore, maintenance of antioxidants of fig fruit during storage is important, because of their health benefits for human. Several strategies have been implemented to maintain bioactive compounds of fruit during stor­ age. Among them, coatings are popular because of their biodegradable and non­toxic materials (Reyes­ Avalos et al., 2016; Allegra et al., 2017). They provide a barrier against gas transfer, which delays ripening and improves taste and texture (Khaliq et al., 2019). The Aloe vera gel compounds are mainly polysaccha­ rides, minerals, sugars, vitamins, and antioxidant agents like phenolic compounds (Rasouli et al., 2019). Application of Aloe vera gel has received increased attention by the food industry due to its effectiveness for increasing shelf­life of fresh prod­ ucts and increasing antioxidant activity (Sogvar et al., 2016). Moreover, Aloe vera gel maintained antioxi­ dant activity of button mushrooms (Mirshekari et al., 2019) and sapota fruit (Khaliq et al., 2019). However, few studies have addressed the effects of edible coatings on quality of fig under cold storage condi­ tions. Application of alginate­chitosan decreased fun­ gal contamination and increased firmness of fig fruit under cold storage (Reyes­Avalos et al., 2016). Thus, the objective of this study was to determine the effects of Aloe vera gel application at different concentrations for maintaining phytochemicals of fig fruit during cold storage. We examined several bene­ ficial phytochemicals (anthocyanin, total phenolic compound, total flavonoid concentration, and ascor­ bic acid), antioxidant activity, and phenylalanine ammonia­lyase and superoxide dismutase activities. 2. Materials and Methods Plant materials and treatments Mature harvested figs (Ficus carica L.), cv. Siyah (black, firm with 13% soluble solids content) grown in Fars Province, Iran, were transported to the Faculty of Agriculture of Yasouj University. Mature leaves of greenhouse­grown Aloe vera plants were excised. The leaf matrix was detached from the outer cortex, and then the hydroparenchyma was mixed in a blender. The mixture was filtered through cheese­ cloth to remove the fibers, and the filtrate constitut­ ed fresh Aloe vera gel (Sogvar et al., 2016). Defect­ free fruits with uniform size and color were divided into four groups, each group received one of four treatments: 1) control (0%), 2) Aloe vera gel 1:3 (25%), 3) 1:1 (50%), and 4) 3:1 (75%). After that, all fruits were placed into plastic trays (285 x 125 x 65 mm) over­wrapped with plastic films [0.02 mm­thick polyvinyl chloride (PVC)]. Trays with fruit were stored at 2±1°C and 85­90% RH for 15 days (cold storage). Analyses were performed after 0, 3, 6, 9, 12, and 15 days of cold storage. Firmness, soluble solids (SSC) and ascorbic acid con‐ tent A digital fruit hardness tester (STEP Systems GmbH, Germany) with a 5­mm diameter probe was used to determine fruit firmness (expressed in Newtons (N). Five g of the homogenate of a compos­ ite sample using a kitchen blender (Nu­777, Nautiunl, Japan) with 40 mL of distilled water was used for analyses of chemical parameters (Ranganna, 1986). Then samples filtered through cotton wool. SSC was measured with a handheld refractometer (Atago­ Pal1, Tokyo, Japan) and expressed as percent. Ascorbic acid content was determined using the 2, 6­ dichlorophenolindophenol dye titration method described by Mirshekari et al. (2017). Five g of fruit tissues homogenized in 90 ml of 3.0% metaphosphor­ ic acid solution. An aliquot of the sample (10 ml) was titrated against 2, 6­dichlorophenolindophenol dye until a pink color persisted for 15 s and results expressed as mg ascorbic acid per 100 g of fresh weight (FW). Anthocyanin and flavonoid concentration (FC) Anthocyanin content in fruit samples was mea­ sured by the pH differential method described by Hassanpour (2015). Two g of samples was added to the 20 ml of methanol containing HCl (1%). The mix­ ture was centrifuged at 17,000 g for 15 min at 4 ◦C. Absorbance of supernatant was measured in a spec­ trophotometer (Shimadzu, USA) at 530 and 700 nm in buffers at pH 1.0 and 4.5, using following formula: A = [(A530­A700) pH1.0 ­ (A530 ­A700) pH4.5] Results were expressed as mg of cyanidin­3­O­glu­ coside equivalents per 100 g of FW. FC was measured according to the method described by Saba and Sogvar (2016). Extraction from four g of the sample was done using 50 ml methanol. One mL aliquot of catechin standard solution (0­100 Mirshekari et al. ‐ Aloe vera gel maintains antioxidants of fig fruit 207 mg L­1) or samples were added to 10 mL volumetric flasks containing 4 mL water. Initially 0.3 mL of 5% NaNO2 was added to the flask, following 0.3 mL of 10% AlCl3 was added after 5 min, and then 2 mL of 1 M NaOH was added to the mixture. Immediately, the solution was diluted to a final volume of 10 mL with water and mixed thoroughly. The absorbance was measured at 510 nm, using a spectrophotometer (UV/Vis Perkin Elmer, Lambda EZ201, USA) and result was expressed as mg catechin equivalents per 100 g of FW. Total phenolic compounds (TPC) and antioxidant activity Fruit extract was prepared using the method described by Ong et al. (2013). Fruit tissue (2 g) was homogenized in a glass tube with 10mL of methanol (80%). The mixture was then incubated at 45∘C for 1 h. For TPC measurement 0.1 mL of the crude extract solution was placed in a test tube and 0.1 mL distilled water in a test tube served as the control (blank). Then six millilitres of water was added to the sample and blank. After that, 0.5 mL undiluted Folin­ Ciocalteu reagent was added to the mixtures. Between 30 s and 8 min later, 1.5 mL saturated sodi­ um carbonate was added. Then 1.9 mL water was added to the solutions to give a final volume of 10 mL and the mixture vortexes and incubated for 2 h at 35∘C. The absorption of TPC was determined at 765 nm using a spectrophotometer. A calibration stan­ dard curve was established using gallic acid. TPC was determined against the standard gallic acid calibra­ tion curve and the absorbance value was converted to mg of gallic acid equivalents (GAE) per 100 gram of fresh weight (mg GAE 100 g­1 FW) (Ong et al., 2013). Antioxidant capacity (ferric reducing antioxidant power (FRAP) and trolox equivalent antioxidant capacity (TEAC) assays were determined spectropho­ tometrically, according to Benzie and Strain (1996) and Kerem et al. (2006), respectively. The results were expressed as Fe2+ equivalents mM kg­1 for FRAP and μM trolox equivalents for TEAC in 100 g of FW. Phenylalanine ammonia‐lyase (PAL) and superoxide dismutase (SOD) activities Fig samples were frozen in liquid nitrogen and then stored at ­80°C until analysis. Each frozen sam­ ple (10 g) was ground with a mortar and pestle and used to determine PAL and SOD activity. Two g of samples was homogenized in a 4 mL solution con­ taining 0.05 mol L­1 Tris­HCl buffer (pH =7.5), 3 mmol L­1 MgCl2 and 1 mmol L­1 EDTA at 4◦C. The homogenate was then centrifuged at 25,000 g for 20 min at 4°C and the supernatant was used as the crude extract for SOD and PAL assays (Maghoumi et al., 2013). Measurement of PAL activity was per­ formed at 290 nm, according to the method described by Aghdam et al. (2012). PAL activity was evaluated as nM cinnamic acid h­1 mg­1 protein. The procedure for assay of SOD was performed using methods described by (Maghoumi et al., 2013). SOD activity was assayed by measuring its ability to inhibit the photochemical reduction of nitro blue tetrazoli­ um. The absorbance by the reaction mixture was read at 560 nm. Concentration of protein of the extracts was determined according to Bradford (1976) with bovine serum albumin as a standard. Enzyme activity was expressed as unit mg­1 protein. Sensory evaluation Texture, taste and overall quality of samples ana­ lyzed by ten trained panelist after 15 days at cold storage (2±1°C) and transferring fruits to the room temperature for sensory analysis. The sensory were evaluated using a hedonic scale 1­5, where 1= very poor, 2= poor, 3= fair, 4= good and 5= excellent. Experimental design and statistical analysis All experiments were conducted within a com­ pletely randomized design (CRD). Data were pooled before analysis and the whole experiment was repeated three times. In each biological and technical experiment 328 fruit were used. There were four replicates per treatment in each experiment. Data were subjected to analysis of variance using the Statistical Analysis System (SAS, ANOVA procedure) version 8.2 (SAS Institute Inc., Cary, NC, USA). The means were compared with the Duncan’s Multiple Range Test (DMRT) at significance level of 0.05. 3. Results and Discussion Firmness, SSC and ascorbic acid content Firmness is the key factor of quality and which changes during ripening (Madani et al., 2014). Fruit firmness was reduced during storage irrespective of treatment, but Aloe vera gel treated fruits softened more slowly (Fig. 1A). Short postharvest life of fig fruit is because of softening and epidermal cracking (Villalobos et al., 2016). Aloe vera film acts as a barri­ er which prevents O2 uptake on fruit, thereby decreases softening and ripening processes (Hassanpour, 2015). Moreover, polygalacturonase and pectin methylesterase activity increases during ripening, and this causes fruit softening (Madani et Adv. Hort. Sci., 2020 34(2): 205­212 208 al., 2014). The results are comparable with Reyes­ Avalos et al. (2016) who indicated that alginate­chi­ tosan coating could maintain firmness of fig fruit dur­ ing storage. Aloe vera gel might decrease polygalac­ turonase and pectin methylesterase activity and thereby maintain firmness of fig fruit during cold storage. There were significant differences in the SSC among treatments. SSC of control fruits increased during storage (Fig. 1B). However, Aloe vera gel treated fruits had the lowest SSC compared to the control during cold storage. The increase in SSC might be related to the solubilization of polyuronides and hemicelluloses of fruit cell walls and hydrolysis of insoluble polysaccharide into simple sugars (Tanada­ Palmu and Grosso, 2005). These results are compara­ ble with Rasouli et al. (2019) and (Martínez­Romero et al., 2017) who mentioned that Aloe vera gel reduced the SSC of orange and plum fruit, respective­ ly. Aloe vera gel might decrease respiration rate and SSC in fig fruit. During cold storage, ascorbic acid content of con­ trol fruit decreased from 24.75 mg per 100 g of FW to 7 mg per 100 g of FW (Fig. 1C). However, Aloe vera gel treated fruits maintained ascorbic acid content relative to the control. Ascorbic acid is the most important antioxidant which decreases the damage of ROS (Rasouli et al., 2019). Autoxidation causes ascorbic acid losses during storage when combines with oxygen in the air (Baraiya et al., 2015). Aloe vera gel might causes a barrier layer for gas and decreases oxidation of ascorbic acid which caused by ascorbate oxidase enzyme in the presence of oxygen (Sogvar et al., 2016). Since ascorbic acid has beneficial effect on human health, the positive effects of Aloe vera gel on maintaining ascorbic acid content of fig fruit can be interested for nutraceutical purposes. Anthocyanin, FC, TPC and antioxidant capacity Fig fruit is rich in phenolic compounds, which are responsible for antioxidant activity (Ercisli et al., 2012). Anthocyanin of non­treated fruits at harvest and after 15 days of cold storage was 11.12 and 21.45 of mg cyanidin­3­O­glucoside equivalents per 100 g FW, respectively. (Fig. 2A). Aloe vera gel 50% and 75% treatments increased anthocyanin after 15 days at cold storage relative to the control. (Fig. 2A). Moreover, FC of Aloe vera gel treatments was signifi­ cantly higher than control during cold storage (Fig. 2B). TPC decreased during cold storage regardless of treatments; but TPC of treated fruits were significant­ ly higher than that of non­treated fruits (Fig. 2C). From a biological and nutritional perspective, the antioxidant capacity of anthocyanin is important (Wang et al., 1996); therefore, maintaining antho­ cyanin is potentially beneficial. It has been also reported that strawberries, and bush blueberry treat­ ed with chitosan maintained higher levels of antho­ cyanin (Wang and Gao, 2013; Chiabrando and Giacalone, 2015). Flavonoids are water soluble polyphenolic mole­ cules which have health promoting effects like antioxidants, radical scavengers, anti­mutagenic, anti­inflammatory, anti­carcinogen, and anti­depres­ sant (Singh, 2016). Moreover, with their antioxidant activity, they increase shelf life of fruits and vegeta­ bles (Ververidis et al., 2007). Nair et al. (2018) showed higher FC in guava fruit treated with chitosan coatings. Also, (Khaliq et al., 2019) indicated that Fig. 1 ­ Firmness (A), soluble solid concentration (SSC) (B) and ascorbic acid content (C) values in figs (Ficus carica L.) ‘Siyah’ fruit treated with Aloe vera gel (0, 25, 50 and 75%). Fruit were stored at 2°C. Vertical bars represent standard error of means of three experiments with four replicates per experiment. Mirshekari et al. ‐ Aloe vera gel maintains antioxidants of fig fruit 209 Aloe vera gel treated sapodilla fruits had higher FC. Phenols are one of the most important antioxi­ dant compounds of fruits and vegetables. The appli­ cation of coatings like Aloe vera gel might delay senescence and decrease TPC loss during storage (Rasouli et al., 2019). Increase in anthocyanin, FC and TPC of fruit treated with Aloe vera gel is comparable to those reported previously by Hassanpour (2015) for raspberry fruit treated with aloe vera gel. This may be related to the persistent biosynthesis of anthocyanin, flavonoids and TPC after harvesting. Also, enzymes which are involved in biosynthesis process of TPC, flavonoids and anthocyanin like PAL might be up regulated with Aloe vera gel treatment. The higher nutraceutical compounds detected in loquat fruits coated with chitosan could be related to Fig. 3 ­ Antioxidant capacity with trolox equivalent antioxidant capacity (TEAC) (A) and ferric reducing antioxidant power (FRAP) (B) in figs (Ficus carica L.) ‘Siyah’ fruit treated with Aloe vera gel (0, 25, 50 and 75%) during cold storage at 2°C. Vertical bars represent standard error of means of three experiments with four replicates per experiment. the lower ROS due to the long­time physiological stress of storage (Petriccione et al., 2015). Therefore, Aloe vera treated fruit might have a protective effect on nutraceutical compounds in delaying their oxida­ tive processes and bio­transformation during stor­ age. Figs treated with Aloe vera gel had higher antioxi­ dant activity during cold storage, which indicated by TEAC and FRAP. However, antioxidant activity of con­ trol fruit decreased during storage (Fig. 3A­B). Serrano et al. (2006) observed that Aloe vera gel treatment increased antioxidant activity in grape. It was supposed that antioxidant activity of Aloe vera gel is related to aloe­emodin, a hydroxyan­ thraquinone present in Aloe vera gel leaves and extracts (Serrano et al., 2006). Therefore, higher antioxidant capacity observed in Aloe vera gel treat­ ed fig fruit could be related to the biochemical com­ ponents of Aloe vera extract. Association was stated between the bioactive compounds and antioxidant activity, with the coated samples recording higher antioxidant activity (Anraku et al., 2011). Fig. 2 ­ Anthocyanin (A), flavonoid (B) and total phenolic concen­ trations (TPC) (C) values in figs (Ficus carica L.) ‘Siyah’ fruit treated with Aloe vera gel (0, 25, 50 and 75%). Fruit were stored at 2°C. Vertical bars represent standard error of means of three experiments with four replicates per experiment. 210 Adv. Hort. Sci., 2020 34(2): 205­212 PAL and SOD PAL activity in treated fruits increased during stor­ age when compared with the control (Fig. 4). This indicates that Aloe vera gel treatment activated enzymes that are important in biosynthetic pathways of secondary metabolites of fruit. PAL is the first enzyme in phenylpropanoid pathway which catalyzes conversion of phenylalanine to trans­cinnamic acid and plays an important role in phenolic compounds biosynthesis (Hassanpour, 2015). PAL connects pri­ mary metabolism (shikimic acid pathway) to sec­ ondary metabolism (phenylpropanoid pathway) (Razavi and Hajilou, 2016). The results are compara­ ble with Hassanpour (2015) who demonstrated that PAL activity in raspberry fruit increased when treated with Aloe vera gel. We suggest that Aloe vera gel treatment might be an efficient strategy for main­ taining phenolic content in fig fruit via activation of PAL. SOD activity of non­treated figs was reduced dur­ ing storage. However, SOD activity increased from day 3 to 6 in cold storage and decreased afterward when treated with Aloe vera gel (Fig. 5). Superoxide dismutases (SODs) which are metalloenzymes, are believed to play a crucial role in antioxidant defense because they catalyze the dismutation of O2 ­ to H2O2. However, defensive action of SOD against O2 ­shows age­related changes. Higher SOD activity of Aloe vera coating treatments have been associated with cold storage stress tolerance fruit because it neutralizes the reactivity of the superoxide radical, which is over produced under stress (Bowler et al., 1992). These results are comparable with Sun et al. (2010) who reported that SOD activity in litchi fruit treated with chitosan was higher than control fruit. These results have suggested that Aloe vera gel treatment might maintain TPC, FC and anthocyanin of fig fruit by increasing activity PAL and SOD enzymes. Sensory evaluation According to the judges, postharvest Aloe vera application did not have any negative effect on tex­ ture, taste and overall quality of fig (Fig. 6). The posi­ tive effect has an important role for consumers to buy the fruit. These results are in agreement with Song et al., 2013 in which Aloe vera gel coated fresh cut apple had higher score than un­coated fruits. Fig. 4 ­ Phenylalanine ammonia­lyase (PAL) activity in figs (Ficus carica L.) ‘Siyah’ fruit treated with Aloe vera gel (0, 25, 50 and 75%) during cold storage at 2°C. Vertical bars repre­ sent standard error of means of three experiments with four replicates determinations per experiment. Fig. 5 ­ Superoxide dismutase (SOD) activity in figs (Ficus carica L.) ‘Siyah’ fruit treated with Aloe vera gel (0, 25, 50 and 75%) during cold storage at 2°C. Vertical bars represent standard error of means of three experiments with four replicates determinations per experiment. Fig. 6 ­ Sensory evaluation in figs (Ficus carica L.) ‘Siyah’ fruit treated with Aloe vera gel (0, 25, 50 and 75%) after tran­ sferring from 15 days in cold storage to the ambient tem­ perature. Mirshekari et al. ‐ Aloe vera gel maintains antioxidants of fig fruit 211 Thus, these results revealed that Aloe vera coting could decrease the loss of the sensory characteristics of fruit. 4. Conclusions This research indicated that Aloe vera gel plays a positive role in maintaining TPC, anthocyanins, FC and antioxidant than control fruit. We conclude that Aloe vera gel treatment could be a useful alternative to the current chemical protocols for preserving nutraceutical traits of fig fruit by maintaining antioxi­ dant capacity during storage. Acknowledgements The authors would like to acknowledge Yasouj University for providing facilities for this experiment. 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