Role of Chitosan in the Coloring of Berries and Phytochemical Changes in Physalis angulata L. During Harvest Maturity

Abstract

Physalis angulata L. berries are green in the initial stage of maturity and turn yellow when fully mature due to an increase in carotenoids. However, the coloration of the epidermis of the berry should not be the reference for harvesting maturity, since the calyx is fully closed. The use of an edible chitosan coating delays the color changes in the berry by reducing the respiration rate. This work studies the effect of harvest maturity and chitosan on the shelf life and berry coloring in Physalis angulata L. Three factors were considered, being harvest maturity stage (green mature (GM), yellowish-green (YG) and yellow (Y)), chitosan coating (0, 0.5, and 1%), and storage time (10, 20, 30 days). The fruits were stored at 20 °C and 85% Rh. The results showed that on the harvesting stage, chitosan coating had a significant effect on the quality and shelf life of berries during storage time. The value of carotenoid and phenol contents, flavor index, chroma, and hue significantly increased with berry maturity. Chitosan delayed the decrease in chlorophyll, phenol contents, antioxidant capacity, berry maturity, and color change. The results show that in the berries coated with 1% chitosan during storage, changes in color were less in comparison with the control condition (no chitosan). The highest decrease of hue angle and color index (17.92°) was observed in the control. The highest total antioxidant (78.42%) was observed after 30 days of storage in MG berries treated with a 0.5% chitosan coating.

1. Introduction

Physalis sp., commonly known as camapu, fisalis, juá-de-capote, or mullaca, belongs to the Solanaceae family, and most of the diverse plants of this genus are found in South America [1]. Physalis angulata L. is known in the Peruvian Amazon as bolsa mucalla or mullaca. The fruit is enclosed in a papery husk or calyx and is 1.5–2.5 cm wide, 4–10 g in weight, with a smooth, waxy, yellow skin and juicy pulp containing numerous small edible seeds. When the fruit is thrown, the calix naturally separates from the plant [2,3]. Fruits contain health-promoting compounds, especially ascorbic acid, B-carotene, phosphorus, iron, protein, and fiber [4].

Berries harvested at the immature stage are more prone to suffer physical damage and transpiration losses during postharvest and have lower quality than fruits harvested at the proper maturity stage [5,6]. Enhancing knowledge of polyamine metabolism during postharvest would be relevant to understand the ripening behavior of fruits [7]. However, fruit harvested at the full maturity stage better maintains its quality, due to the high acidity and lower weight loss [8]. Overripe fruits, which are very soft with a floury texture and insipid flavor soon after harvest, are caused by a delay in harvesting. Rufato (2008) recommended the collection of Physalis sp. for human consumption when the cup is yellow in color, because this would ensure a better-quality berry [9]. The color of the berries is a primary quality factor, as vision is the first sense to be used and visual appreciation is crucial in selection [10,11]. In addition, berry color is the visual manifestation of organic compounds such as anthocyanins and carotenoids, which accumulate mainly in the peel and occasionally in the pulp. The color and stability of these compounds are affected by pH, light, temperature, and texture [12,13]. Fischer and Martinez (1999) [14] classified Physalis sp. for consumption after harvesting it into six classes according to the color of the epidermis: green, orange-yellow, light orange, orange, dark orange, and reddish orange. The last three classes have the best physicochemical characteristics for consumption [15].

In recent years, consumer preferences have changed with the demand for lower levels of chemical preservatives (or antimicrobials) and greater reliance on foods with more natural and fresh characteristics [16,17]. Therefore, researchers have been investigating safer alternative substances with environmentally friendly properties to reduce the use of synthetic fungicides in fruits [18,19]. Edible coatings (which mainly consist of proteins, lipids, or polysaccharides) are considered an environmentally friendly technology to extend the shelf life of fruit through the reduction of moisture loss and the respiration rate, thus preventing physical damage and enhancing the appearance of the product [20].

The use of edible coatings is one of the environmentally friendly technologies that is used to minimize moisture loss, oxidation, or gas exchange processes, thereby improving the quality and shelf life of fruits [21]. Chitosan is a biodegradable and biocompatible polymer derived from natural renewable resources. It has numerous applications in various fields, one of which is the area of edible films and coatings. Furthermore, chitosan cannot penetrate into tissues within muscle organs or even fruit cover due to its insolubility in water, and therefore appears as a safe physical modulator of the fruit biological system [22,23]. These complexities offer an interesting potential for use with fresh foods. Chitosan derivatives have been widely applied because of their several advantages due to their prominently active amino groups [24,25]. Recently, a chitosan coating has been applied to maintain the postharvest quality of fruits, preserving fruit color and biochemical properties in Prunus domestica [26], Pyrus communis L. [27], Mangifera indica L. [28], and Vaccinium angustifolium [29], and achieved satisfactory responses.

To our knowledge, little information is available regarding the effect of chitosan coating on berry coloring in Physalis angulata L. at storage time. Therefore, the aim of this study was to investigate the effect of harvest maturity and chitosan coating on the change in the color, some important quality characteristics, and antioxidant properties of the Physalis angulata L. berries kept at 20 °C for 30 days.

2. Materials and Methods

2.1. Plant Materials and Treatments

Physalis berries (Physalis angulata L.) were harvested in three different ways with the shape, color, and size recommended by Rufato (2008) for fresh consumption. The berries (green mature (GM), yellowish-green (YG), and yellow (Y)) from plants cultivated on the research farm of the University of Zanjan, Iran were harvested and transferred to the laboratory on the same day. The pieces of berries were selected based on uniformity, shape, color, and size. The berries were first weighed, and then medium-sized berries were used, while diseased berries were discarded [9]. For treatment with chitosan, first the calyx was removed from the berries, and then the treatment was performed.

2.2. Materials and Instruments

Chitosan (Foconsci Chemical Industry Co., Ltd., Zaozhuang, China), was prepared at three different concentrations, 0, 0.5, and 1% (w/v), in an aqueous solution of acetic acid (0.5% v/v). A chitosan (C₁₂H₂4N₂O₉) medium-molecular-weight-tested (degree of deacetylation 75–85%, CAS number: 9012-76-4, Product Number: 448877, viscosity 200–800 cP, 1 wt. % in 1% acetic acid at 25 °C, (Fanavaran Petrochemical Company, Tehran, Iran)) concentration of 1.0% was prepared by dissolving 10 g of chitosan in 1000 mL of distilled water, gradually adding 10 mL of acetic acid. The final pH was 5.6. The solution was heated and constantly agitated for 24 h (Tween (2%) was used as plasticizer). The final solution was adjusted to 1000 mL of distilled water. After cooling at 20 °C, the berries (15 berries per each sample) were dipped in the chitosan solution for 60 s to allow the chitosan to adhere to the whole berry surface to create a uniform film. Samples were dried at room temperature. A control group (15 berries per sample) was created by dipping berries in distilled water. The average amount of chitosan, which covered the fruit, for the 1% group was 125 mg/100 g, whereas in the 0.5% group it was 57 mg/100 g. Then, the berries were stored in separate packages (15 berries per package) at a temperature of 20 °C and a relative humidity of 85% for 30 days. At 10-day intervals, a group was taken at random and transferred for 1 day at 25 °C (shelf life) and subjected to physicochemical analysis.

2.3. pH, Titratable Acidity (TA), Total Soluble Solids Content (TSS), and TSS/TA Assessment

The berries’ juice was extracted using a juicer. Juice was filtered with cheesecloth to separate seeds and skins, and the fresh berry juice was analyzed directly after production. The pH values of the solutions were monitored with a pH meter [30]. Titratable acidity (TA) was determined by titration of 10 mL of diluted extract in 25 mL of distilled water to pH 8.2 using 0.1 N NaOH. The amount of berry (berry juice) used was equal to 10 mL [31]. TSS was measured using a digital refractometer (RX5000A; ATAGO Co., Ltd., Tokyo, Japan). All readings were temperature-corrected to 20 °C [32]. The ratio of sugar to acid, which determines the taste of berries, was evaluated through the ratio of TSS to TA [33].

2.4. Weight Loss Assessment

Berries were weighed on day 0 and at the end of each storage interval. Weight loss was calculated as the percentage loss of weight with respect to the initial weight.

2.5. Preparation of Berry Powder to Measure Phenol, Flavonoids, and Antioxidant Properties

The berries were dried in an oven at 40 °C for 96 h, and then the dried material was milled. After this, 1 g of each sample was soaked in 50 mL of 80% methanol for 48 h at room temperature. After the specified time, the extracts were straightened with Wattman No. 4 filter paper. The solvent was evaporated at a temperature below 55 °C. The remaining experiments were conducted at 4 °C [34].

2.5.1. Total Phenol Content

To measure the total phenol content, 2 mL of sodium carbonate (2%), 2.8 mL of distilled water, and 100 µL of Folin–Ciocalteu phenol reagent (50%) were added to 100 μL of plant extract. After 30 min, their absorbance was recorded at a wavelength of 720 nm compared to the control. Gallic acid was used as a standard for drawing a standard curve. The total phenol content of the extracts per mg (the equivalent of glycogen acid per gram of dry weight of the plant) was reported [35].

2.5.2. Flavonoid Content

To measure the total flavonoid content, 1.5 mL of methanol (80%), 100 μL of aluminum chloride solution (10%), 100 μL of sodium acetate solution of 1 M, and 2.8 mL of distilled water were added to 500 μL of each extract. The absorbance of the solution was measured over 40 min in a 415 nm wavelength range compared to the control. Blank contains all of the above ingredients, but instead of the extract, the same amount of methanol was added at an 80%. Quercetin was used to draw the standard curve. The total flavonoid content of the extracts was reported in mg equivalent to quercetin per gram of dry weight of the plant [36].

2.5.3. Total Antioxidant Capacity

Based on the DPPH method [37], various concentrations (final mass ratios of extracts with DPPH were approximately 3:1, 1.5:1, 0.75:1) of the extract were mixed with 2 mL of methanol solution (DPF) of 0.004%. The blank contained 2 mL of DPPH and 2 mL of methanol. The solutions were stored for 30 min in the dark at room temperature. The absorbance of the samples was found to be 517 nm compared to the methanol control. The percentage of free radicals (I%) in each extract was calculated using the following formula:

%I = ((A _CONTROL − A _SAMPLE)/(A _CONTROL)) × 100

2.6. Berry Color Assessment

The RGB device (Lutron-RGB-1002, MICRONIX Company, Praha, Czech Republic) was used to evaluate the color of the berries. For this purpose, 5 out of 15 berries were randomly selected, and 5 parts from each berry were measured. The R(red), G(green), and B(blue) color’s values were then obtained using the data collected for each sample. With the Convert RGB to Lab software, the white color indices were determined (from http://colormine.org/convert/rgb-to-lab, V.1.1, accessed on 2 May 2019). Based on the values of L, a, and b, the color difference indices (ΔE), C (chroma), and H (hue) were calculated. L means the lightness from 0 (black) to 100 (white). The chromaticity value a is red when positive and green when negative. The chromaticity coordinate b is yellow when positive and blue when negative [10].

2.7. Total Chlorophyll and Carotenoid Content

Chlorophyll and carotenoids were analyzed using the Arnon method (1975). Chlorophyll and carotenoids were extracted from a sample of 1 g fresh berry pericarp in acetone 80% (v/v). Absorption was measured at 645 and 663 nm for chlorophyll and 480 and 510 nm for carotenoids using a spectrophotometer (UV-600) (HACH Company, Loveland, CO, USA) [38]. Total chlorophyll and carotenoids were expressed as 100 mg g⁻¹ fresh weight and determined using the formula:

Total chlorophyll (mg gFW⁻¹) = [20.2 (A₆₄₅) + 8.02 (A₆₆₃)] × V/W 1000

Carotenoids = [7.6 (A₄₈₀) − 1.49 (A₅₁₀)] × V/W 1000

A: absorption

V: acetone volume used

W: weight of fresh berry pericarp

2.8. Statistical Analysis

The experimental design was a three-way ANOVA conducted to check the interaction effects between the factors with 3 repetitions per treatment. There were 3 levels of the harvest stage factor (GM, YG, and Y), 3 levels of chitosan treatment (0, 0.5, 1% chitosan), and 3 levels of the storage time factor (10, 20, 30 days). Statistical analyses were performed with SPSS software package v. 20.0 for Windows (SPSS Inc., Chicago, IL, USA), and means comparison was carried out by Duncan’s multiple range tests at p < 0.05. Differences at p < 0.05 were considered significant and indicated by different letters. The data are expressed as the mean ± standard deviation.

3. Results

3.1. pH

The pH value of the berries increased significantly during berry maturity. The results indicated that in Physalis berries, the highest pH (4.99) was recorded in berries harvested at stage Y after 30 days of storage (Figure 1a). The chitosan coating treatment had a significant effect on the pH. In Physalis berries, the pH increased over the storage period, reaching its maximum at 30 days; however, this increase was observed in the control samples (without chitosan coating) rather than in the treated berries (Figure 1b).

3.2. Weight Loss Analysis

Our data showed that chitosan significantly reduced the weight loss during storage. The highest weight loss in 30 days after storage occurred in control berries, and the lowest weight loss 10 days after storage (0.371%) was observed in those with 1% chitosan coating (Figure 2b). The weight loss of MG berries was significantly (p < 0.01) higher than at the two stages of puberty (YG and Y) during storage. The highest percentage of weight loss for MG berries was observed after 30 days of storage (9.2%) (Figure 2a). The lowest weight loss (0.945%) was observed for the berries harvested in the Y stage (Figure 2a). The results of this study indicated that the highest weight loss (11.36%) was observed in the berries harvested in the GM (control) (Figure 2c). The lowest percentage of weight loss in the berry harvesting (Figure 2c) was observed in the YG and Y stages (1.83 and 1.91%) with 1% chitosan coating.

3.3. Titratable Acidity (TA), TSS, and TSS/TA

During the maturity of the berry at all levels of chitosan coating and the harvest stage during storage, the TA decreased, but TSS increased (Table 1). Although during storage the TA content was reduced, in the berries treated with chitosan, the reduction was less than in the control berries, and thus the highest amount of TA (0.867%) was found in MG Physalis berries at 0.5% chitosan within 30 days of storage (Table 1). Also, berries harvested in the Y stage without chitosan coating had the lowest amount of TA (0.37%) after 30 days of storage (Table 1). Unlike TA, the TSS content in Physalis berries increased during storage and was lower in chitosan-treated berries than in the control berries (Table 1), so that the highest amount of TSS was found in MG Physalis berries without chitosan within 30 days after storage (Table 1).

In the study of taste index, the results indicated that as the total soluble solids (TSS) increased, the taste index value also rose. This is attributed to the increase in TSS and the decrease in titratable acidity (TA) associated with the maturity of Physalis berries. Consequently, the taste index increases with higher TSS levels during berry ripening (Table 1).

3.4. Total Phenolic (TPC) and Flavonoid Content (TFC)

The results of this experiment show that the amount of TPC increased significantly (p < 0.01) with berry maturity, and berries harvested in the Y stage exhibited higher TPC at the harvest time (Table 1). The TPC of berries harvested at the GM stage increased during the storage time. The value of TPC in the berries harvested at the YG and Y stages increased for the first 20 days, decreasing afterward. The results indicated that the chitosan coating treatment increased the total phenolic content (TPC) for up to 20 days, after which it began to decline until the end of the storage period. A TPC of 3.33 mg g⁻¹ dry weight (DW) was recorded in the berries at the yellow-green (YG) stage with a 0.5% chitosan coating on the 30th day of storage. (Table 1).

The TFC significantly (p < 0.01) increased with berry maturity but was reduced during storage (Table 1). As shown in Table 1, the TFC of control berries harvested at the GM stage increased during early storage, reached a peak at the 10th day of storage, and then decreased. In the YG-stage berries, the TFC decreased until the 20th day and then increased for 30 days, which had no significant difference with harvest time. On the other hand, the TFC of the berries harvested in stage Y showed a decrease during storage time (Table 1). The results of the present study also showed that postharvest chitosan treatment decreased the TFC value as compared to that of control berries.

In general, the highest level of TFC (8.19 mg g⁻¹ DW) was observed in berries harvested in the Y stage at harvest time, and the lowest TFC content (2.69 mg g⁻¹ DW) was observed in the berries harvested at the Y stage without chitosan coating after 30 days of storage.

3.5. Effect of Treatment on Antioxidant Capacity

The results of this experiment show that the amount of antioxidant capacity significantly (p < 0.01) decreased with berry maturity, and berries harvested at the GM stage exhibited a higher antioxidant capacity at the harvest time (Table 1). Generally, the antioxidant capacity at all levels of the chitosan coating and harvesting stage decreases during storage; considering that the control samples had the lowest antioxidant capacity, there was a significant difference between levels of chitosan. Also, in GM berries, those treated with chitosan had the highest levels of antioxidant activity, at 0.5% after 30 days. Based on the results of this study, with the berries’ maturity, their antioxidant capacity decreases (Table 1).

3.6. Effect of Different Treatment Chlorophyll Content (TChl)

With the maturity of the berry and during the shelf life, the TChl of the berry decreased (Table 2). The highest amount of TChl was obtained from the berries harvested at the MG stage at harvest time (42.55 mg 100 g⁻¹ FW) (Table 2). The lowest TChl (4.75 mg 100 g⁻¹ FW) was observed in berries harvested at the Y stage 30 days after storage (Table 2). During the storage period, despite the decrease in TChl, at the MG stage, using different chitosan coating levels, the process of TChl reduction slowed down, and after 30 days the highest TChl was recorded (17.22 mg100 g⁻¹ FW) in berries coated with chitosan, at a level of 0.5% (Table 2).

3.7. Carotenoid Content

The level of carotenoid content increases with berry maturity (Table 2). Also, the results showed that at all levels of the chitosan coating and harvesting stage, carotenoid content was reduced during the storage period. The highest carotenoid content in the berries harvested at the yellow (Y) stage was observed in those treated with chitosan coatings at 1% and 0.5% levels, showing carotenoid contents of 68.17 mg 100 g⁻¹ fresh weight (FW) and 58.87 mg 100 g⁻¹ FW, respectively, after 10 days of storage. After 30 days, the lowest carotenoid content (4.40 mg 100 g⁻¹ FW) was found in control samples of berries harvested at the Y stage. (Table 2).

3.8. Effective Treatments Berry Coloring

3.8.1. Chroma Index

Our results show that chroma index significantly (p < 0.01) increased during storage and maturing (from the MG stage to Y stage) of the berries, from harvesting to 30 days after storage; However, this increase was significant in both chitosan-coated berries and control samples during the storage period. Different levels of chitosan coating delayed berry maturity during storage and slowed down the rate of color change in the berry. The highest chroma index (57.06%) was observed for the berries harvested in the Y stage (without chitosan coating) after 10 days of storage. The lowest chroma index was observed in berries harvested at the mature green (MG) stage during the harvest (Table 2).

3.8.2. Hue Angle

Our results showed that the amount of hue angle significantly (p < 0.01) increased with berry maturity, and berries harvested at the Y stage exhibited a higher hue angle at the harvest time. The hue angle in Y decreased during storage. In the YG stage, coating with chitosan prevented the increase in hue angle during storage, and the maximum hue angle was observed in YG-stage berries without chitosan coating after 30 days of storage. The highest hue angles in these two stages of harvest were 76.78° and 76.21°, respectively. The MG-stage berries’ lowest hue angle (68.76°) was observed at harvest time (Table 2). During maturation and storage, the hue angle in MG-stage berries increased, and this increase was greater in the control than in berries treated with chitosan at the level of 0.5 and 1%. In general, during berry maturity and storage, the greatest change in the hue angle was observed in the control plants and in the MG stage, which indicates that the color of the berry shifted from green to yellow during the period of examination (Table 2).

3.8.3. Color Change Index

The color change index during storage was accompanied by a positive trend, which showed a significant difference in the green berry of the YG and ripe berry (Y stage) (Figure 3a). The results show that in the berry coated with 1% chitosan during storage, the changes in the color of the berries were less than in the control berries (Figure 3b). The rate of color change in the berries harvested in the MG stage was significantly higher than that in the two stages of puberty (YG and Y) during storage. The highest color change index value for berries harvested in the MG stage after 30 days of storage was 17.92°. The lowest index value of color change in berries harvested in the Y stage (9.56°) was observed after 10 days of storage (Figure 3a).

4. Discussion

The present study aimed to investigate the effect of the harvesting stage and edible chitosan coating on the coloring of Physalis angulata L. berries during harvest maturity. In evaluating the quality of berries, color is considered a very important index; the consumer first evaluates this qualitative feature at the berry selection stage. Color is considered to be a major quality aspect of unprocessed and processed foods, and its changes reflect chemical changes due to storage processes such as browning, frying, and drying [39]. During plant maturity, phytochemical changes affect antioxidant activity and affect the quality of the nutrition of different types of fruits and vegetables at specific times [40]. Analysis of variance of the data obtained from the evaluation of changes in physicochemical traits of Physalis angulata L. berries during storage is presented in Table 1. The data are based on physicochemical changes in the first 30 days of storage or during the entire storage period. The results indicate that different levels of chitosan coating, harvest stage, and storage time significantly affect the total soluble solids (TSS), titratable acidity (TA), TSS/TA ratio, and overall quality during storage.

Chitosan treatment can restrict water transfer or dehydration, gas exchange, and nutrient loss by acting as a protective barrier, and thus reduce weight loss of postharvest fruit [41]. Weight loss in fruits during storage time, one of the important factors that affect the appearance and quality of harvested fruit, results from evaporative water loss or respiratory processes [42]. In our study, the lowest percentage of berry weight loss in harvested berries was observed in the Y stage, with 1% chitosan coating, during storage time (Figure 2c). In agreement with our study, Lin et al. (2018) show that in Dimocarpus longan Lour., weight loss treated with chitosan was slower than that of untreated berries within the postharvest storage [43].

Based on the results related to the growth stages of the Physalis angulata L. berries, with berry maturity, the amount of chlorophyll content was reduced, and during the storage period, the amount of carotenoids followed a decreasing trend. In this study, total carotenoid variation with the growth and storage time of the plant was significant; thus, the adult berry had the highest level of carotenoids. During the maturity of the berry and the berry storage, the greatest change in the hue angle was observed in the control plants and in YG berries (Table 1), which indicates that the color of the berry shifted from green to yellow during the period of examination. Certainly, the reduction in the hue angle for ripe and Y-stage berries can be due to the deterioration of the carotenoids present in the berries during storage. Further, environmental factors such as temperature, oxygen, and ethylene affect the degree of chlorophyll change [44]. For further studies, it might be a good idea to test the effects of coating and maturity on the ethylene responsiveness of the Physalis sp. Also, for postharvest research in fruit, it could be interesting to add this information and consider it in the discussion, especially regarding the effects of ethylene.

Color parameters (chroma index, hue angle, browning index, color change index, etc.) are used to evaluate the changes in fruit color during storage and fruit ripening. According to the results, due to the climacteric of the Physalis berries and the gradual ripening and discoloration of the berries, the berries harvested in the MG stage compared to those harvested at YG and Y increased the storage time at 15 °C to 30 days. Also, during storage, the color change index of MG berries was higher than that of berries harvested in the YG and Y stages. However, the use of chitosan coating slowed the color change in treated berries compared to untreated berries. In agreement with our study, Shah and Hashmi (2020) showed that during storage time, mango color changed from green to pale yellow [45]. Control treatment showed a faster change, while a steady color variation was observed in chitosan-coated treatments, and coated mangoes retained color, with significantly (p ≤ 0.05) higher hue angle values for chitosan-coated mango berries. The difference in L*, C*, and hue angle values of the berries is due to different levels of various coloring pigments. Chitosan coating delayed the development and coloring pigments in mango fruit. Explanations for this result may be attributed to the yellow color associated with the carotenoids present in Physalis berries, and discoloration of the fruit may be due to pigment degradation by the action of hydrolytic enzymes that, by breaking down the linkage of the glycosidic substituent in the moieties, lead to loss of color during postharvest storage [46,47].

Increased pH of the fruit is due to its biochemical activity, which causes the organic acid contained in the fruit to be converted into sugary products. The results are consistent with the results of Wells (2002) [48], who stated that the acidic changes of fruit extracts at the time of ripening are due to the leakage of organic acids from the vacuoles in the cellular cytoplasm, which undergoes changes in berry pH and TA. It can be said that in Physalis, with ripening of the berry, its pH increases and, as a result, the TA of the berry decreases. The study of pH and TA of berries indicates that the TA was decreased by berry maturity and prolonged storage time. The increase in TSS/TA and total phenol content during storage can be due to a significant reduction in TA (for TSS/TA) and the destruction of the berry cell (for total phenol content) [49]. In the present study, the increase of the TSS/TA in berries can be due to the loss of much of the berry water, and consequently the condensation and rise in TSS in berries during storage and consumption of high levels of organic acids. Additionally, during storage, the decrease in TA level is accompanied by an increase in sugars, part of which may be due to the conversion of acids to sugars [50]. The results are consistent with the results of the study of Oke et al. (2013) [51]. This increase can be attributed to the effects of aging, as well as the conversion of acids to other substances, such as sugars [52]. Some researchers also found that the TA was reduced due to its use in respiration and the transformation of tartaric acid into other materials during the storage period [53]. On the other hand, in fruits coated with different concentrations of edible coating, more acidity was retained than in the control, confirming the results of Rasouli et al. (2019) in Citrus sinensis L. Osbeck fruits [54]. This may be due to the slow conversion of acids to sugar upon maturity [55]. Organic acids usually decrease during fruit storage due to consumption in respiration and convert to sugars, and their reduction is directly related to metabolic activity. Reducing the amount of acid during the storage of the fruit in the coating can be due to the fermentation or breakdown of acid into sugar during respiration [56].

It appears that the effects of growth and maturity in total phenol and flavonoid content differ between fruits and vegetables [57], as the level of phenolic and flavonoid compounds in response to maturity of fruits in Capsicum annuum L. [58], Vacciniumcor corymbosum L. [59], and Cornus mas L. fruits [60] decreased, while in Solanum lycopersicum L. [61] these compounds increased. The results of a recent study indicate that the accumulation of flavonoid compounds in the leaves and the vegetative stage began after flowering. Thus, the highest amount of these compounds in the plant of the Physalis angulata L. is related to the flowering and reproductive leaves [62].

Changes in the total phenol content of fruit in the postharvest period depend on various factors such as genotype, stage of harvest, variety, growing season conditions, storage life, and storage time. Phenolic compounds are potent inhibitors of oxidative stress and participate in the collection or removal of hydrogen peroxide in collaboration with peroxides. In this study, chitosan was also affected by the increase in phenol compounds relative to the control. Apart from the type of treatment, total phenol reduction in this experiment is consistent with the methods used in the previous research. The total phenol content decreases with increasing storage time due to the use of phenols to deal with biological and nonbiological stresses such as chilling, etc. [63,64]. Chitosan coating also causes a change in the atmosphere around the fruit, reducing O₂ and CO₂, resulting in latency in the activity of the enzyme phenylalanine aminolyase, which is one of the enzymes needed for the synthesis of phenolic compounds [65]. The difference in results could be due to different concentrations and different gas exchange rates at different levels of chitosan coatings.

Based on the results, it is deduced that the antioxidant capacity of the berries of Physalis angulata L. is reduced with the maturity of the berry, which may be a reason for the reduction in the amount of vitamin C during storage and maturation in these berries. The amount of antioxidant capacity of the berry decreases with the activity of the polyphenol oxidase and the activity of the peroxidase. Also, fruit coatings reduce the activity of these enzymes by reducing the oxygen content in the atmosphere around the fruit and help maintain the antioxidant capacity [66]. Therefore, according to the percentage of different compounds and their antioxidant properties against different oxidants, plant harvesting can be carried out at an appropriate development stage to deal with certain oxidants.

5. Conclusions

The results of our research indicate that the effects of different chitosan concentrations depend on storage time and harvest stage. Also, the amount of phenolic material, carotenoids, hue angle, and chroma index increased with berry maturation but decreased during storage. The results also showed that treatment of the berry with chitosan maintained or delayed reduction of postharvest berry quality. Furthermore, the results showed that in all stages of harvesting (M, YG, and Y stage), different levels of chitosan coating during storage time had significant effects on the quality and shelf life of berries. In addition, our results showed that under normal storage conditions (without treatment), the weight of the fruit changes dramatically in the M stage. On the other hand, during the yellow-green (YG) stage, the berries exhibit the best quality in terms of color, total flavonoid content (TFC), and total phenolic content (TPC), which can be maintained for up to 20 days. Also, the results show that it is possible to delay the amount of weight loss and fruit coloring with chitosan coating. Using chitosan at 0.5% while increasing the storage period has the best effect on the examined traits, such as color and other biochemical structures.

Author Contributions

Z.G., T.B., V.R., M.T.G., S.N., K.W. and M.A. contributed to the design of the study, data interpretation, and manuscript editing. R.H.G. and A.S. performed the experiments, analyzed the data, and wrote the initial draft of the article. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data will be available based on request.

Acknowledgments

We appreciate the Polish National Agency for Academic Exchange (NAWA) Ulam 2021 program (grant number BPN/ULM/2021/1/00250/U/00001) for supporting this study.

Conflicts of Interest

The authors declare no conflicts of interest.

Footnotes

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Figures and Tables

Figure 1. Effects of harvest stage and storage time (day) (a) and chitosan and storage time (b) on pH of Physalis angulata L. berries. Harvest stage: green mature (GM), yellowish green (YG) and yellow (Y); chitosan coating: 0, 0.5, and 1%. Whiskers indicate standard deviation; the values marked with the same letter do not differ significantly according to the Duncan’s multiple range tests (p [less than] 0.05).

Figure 2. Effects of harvest stage and storage time (day) (a), chitosan and storage time (b), and harvest stage and chitosan (c) on weight loss (%) of Physalis angulata L. berries. Harvesting stage: green mature (GM), yellowish green (YG), and yellow (Y); chitosan coating: 0, 0.5, and 1%. Whiskers indicate standard deviation; the values marked with the same letter do not differ significantly according to the Duncan’s multiple range tests (p [less than] 0.05).

Figure 3. Effects of harvest stage and storage time (day) (a) and chitosan and storage time (b) on color change index in Physalis angulata L. berries. Chitosan coating: 0, 0.5, and 1%. Whiskers indicate standard deviation; the values marked with the same letter do not differ significantly according to the Duncan’s multiple range tests (p [less than] 0.05).

Table 1

Changes in some traits under the influence of chitosan in Physalis angulata.

TPC	Antioxidant Capacity (%)	TFC	TSS/TA	TSS	TA (%)	ST (Day)	Chitosan (%)	HS
(mg g−1 DW)		(mg g−1 DW)
0.84	87.85	4.15	2.30	4.13	1.58		-	MG
1.85	74.79	6.13	4.52	4.96	1.086	0	-	YG
2.41	69.14	8.19	6.16	5.8	0.941		-	Y
1.61 hi	74.52 b	5.28 bc	4.1 jk	4.83 kl	1.095 b	10	0
2.33 fg	62.23 e	4.16 e	6.84 gh	6.8 cd	1.072 b	20
2.76 de	47.73 gh	4.71 cd	11.87 a	7.833 a	0.585 g	30
1.156 jk	78.42 a	4.85 cd	3.72 kl	5.13 ij	1.28 ab	10	0.5	MG
2.13 gh	67.35 cd	3.52 f	5.86 hi	5.6 ij	1.105 b	20
2.94 cd	53.25 f	5.36 bc	9.61 ab	7.6 ab	0.867 cd	30
1.43 ij	76.77 ab	4.54 d	3.07 kl	4.73 kl	1.37 a	10	1
1.92 hi	67.32 cd	4.90 cd	4.9 jk	7.6 ab	1.201 ab	20
3.28 ab	51.92 f	5.5 b	8.25 cd	6.6 de	0.688 e	30
2.66 de	67.26 cd	4.0067 ef	5.62 hi	6.066 ef	1.109 b	10	0
3.28 ab	57.35 ef	4.14 e	8.04 de	6.4 de	0.892 cd	20
1.46 ij	41.84 i	6.33 a	10.59 ab	6.5 de	0.545 h	30
2.87 cd	69.67 c	4.34 de	4.966 jk	5.63 gh	1.141 ab	10	0.5	YG
3.38 a	58.45 ef	4.78 cd	6.553 gh	5.96 ef	0.990 bc	20
2.48 fg	45.12 hi	5.51 b	7.976 de	6.03 ef	0.810 de	30
3.38 a	64.77 d	4.82 cd	4.726 jk	5.4 ij	1.171 ab	10	1
2.8 cd	58.13 ef	4.39 de	5.61 hi	5.8 gh	1.002 bc	20
1.58 hi	44.41 hi	4.33 de	6.56 gh	5.9 ef	0.648 ef	30
3.2 b	62.56 e	4.59 d	8.12 cd	7.26 bc	0.987 bc	10	0
2.98 cd	45.85 hi	3.62 f	8.9 bc	6.96 cd	0.825 d	20
2.3 gh	33.17 k	3.22 g	11.44 a	6.93 cd	0.507 i	30
2.49 fg	65.44 d	5.97 ab	7.33 ef	6.06 ef	1.01 bc	10	0.5	Y
3.19 b	49.57 g	5.01 c	7.94 de	6.2 ef	0.877 cd	20
3.33 a	37.21 j	3.56 f	9.27 bc	5.73 gh	0.618 f	30
2.65 de	49.70 g	5.17 bc	7.17 ef	6.7 cd	1.141 ab	10	1
2.97 cd	46.07 h	3.43 fg	7.65 ef	6.13 ef	0.939 c	20
2.04 gh	37.14 j	2.61 h	8.47 cd	5.86 gh	0.612 f	30
						ANOVA
ns	*	*	*	*	*	ST
ns	*	ns	**	**	ns	C
*	**	*	*	*	**	HS
**	*	**	**	**	**	ST × C
ns	ns	ns	*	ns	*	HS × ST
*	**	*	*	*	**	HS × C
**	**	**	**	**	**	HS × ST × C

C: chitosan, HS: harvesting stage, ST: storage time, MG: mature green, YG: yellowish green, Y: yellow. The values marked with the same letter do not differ significantly according to the Duncan’s multiple range tests (p < 0.05). ns: not significant, * p < 0.05, ** p < 0.01.

Table 2

Color changes of berries during storage under the influence of chitosan in Physalis angulata L.

Hue Angle (°)	Chroma Index	Chlorophyll Content (mg·100 g−1 FW)	Carotenoid Content	ST (Day)	C (%)	HS
			(mg·100 g−1 FW)
68.87	38.1	38.1	21.06		-	MG
78.42	48.49	48.49	31.5	0	-	YG
81.89	49.41	49.41	39.26		-	Y
83.45 c	46.49 e	46.49 e	37.07 d	10	0
83.28 c	51.90 cd	51.90 cd	16.120 ed	20
85.62 b	52.13 c	52.13 c	9.83 h	30
81.22 cd	43.48 f	43.48 f	37.67 d	10	0.5
80.55 cd	47.84 e	47.84 e	37.09 d	20
79.44 d	45.26 ef	45.26 ef	9.49 h	30		MG
71.9 e	43.78 f	43.78 f	37.87 d	10	1
77.6 d	44.69 ef	44.69 ef	11.45 g	20
77.74 d	46.43 e	46.43 e	11.74 g	30
82.57 c	51.49 cd	51.49 cd	58.47 c	10	0
87.54 ab	52.13 c	52.13 c	14.75 f	20
88.02 a	52.73 c	52.73 c	6.043 j	30
84.55 bc	36.13 gh	36.13 gh	68.013 ab	10	0.5
79.55 cd	50.21 d	50.21 d	8.75 hi	20		YG
76.97 d	43.40 fg	43.40 fg	6.12 j	30
76.84 d	39.53 g	39.53 g	65.77 b	10	1
87.94 a	39.58 g	39.58 g	10.44 gh	20
77.88 d	27.58 h	27.58 h	8.54 hi	30
85.52 b	57.06 a	57.06 a	68.80 ab	10	0
84. 55 bc	50.92 d	50.92 d	18.75 e	20
82.37 c	45.95 fg	45.95 fg	4.40 k	30
87.20 ab	51.42 cd	51.42 cd	73.39 a	10	0.5	Y
86.74 ab	54.62 bc	54.62 bc	8.76 hi	20
84.77 bc	42.95 gh	42.95 gh	7.10 i	30
76.81 d	50.77 d	50.77 d	74.87 a	10	1
87.61 ab	53.98 bc	53.98 bc	8.21 hi	20
83.13 c	52.81 c	52.81 c	10.09 gh	30
				ANOVA
**	*	*	*	ST
**	**	*	ns	C
**	**	**	**	HS
**	**	*	**	ST × C
**	ns	**	**	HS × ST
ns	**	*	**	HS × C
**	**	**	**	HS × ST × C

C: chitosan, HS: harvesting stage, ST: storage time, MG: mature green, YG: yellowish green, Y: yellow. The values marked with the same letter do not differ significantly according to the Duncan’s multiple range tests (p < 0.05). ns: not significant, * p < 0.05, ** p < 0.01.

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