Melatonin Prolongs the Postharvest Storability of Strawberry Fruits through Reduced Oxidative Stress and Improved Enzyme Activity

Author:
İbrahim Kahramanoğlu Department of Horticulture, Faculty of Agricultural Sciences and Technologies, European University of Lefke, Northern Cyprus, via Mersin 10 Turkey, 99780

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Abstract

Strawberry fruits are popular among consumers because of their unique flavor and reported health benefits. However, microbial growth and oxidative stress that occur in postharvest storage cause strawberry fruits to have a relatively short postharvest life, which reduces consumer acceptance. This study aimed to evaluate the effects of exogenous melatonin application on the enzymatic activity and postharvest quality of strawberry fruits that are stored at 4 ± 0.5 °C. A total of 288 fruits with four replicates for each of the three treatments (control, 200 μM melatonin, and 500 μM melatonin) were used. Several quality metrics were regularly assessed at 3-day intervals during the 18-day storage trials. The results suggested that the exogenous melatonin application significantly increased the activity of antioxidant enzymes at the physiological level, including catalase, ascorbate peroxidase, superoxide dismutase, and peroxidase which led to reductions in weight loss, the decay incidence, and the malondialdehyde level. The use of melatonin successfully delayed changes in the soluble solids concentration, ascorbic acid, titratable acidity, and fruit firmness. The results indicated that applying 500 μM melatonin to strawberries would be a useful strategy for increasing their shelf life.

Strawberry fruits are incredibly popular among consumers because of their exceptional flavor and array of health benefits, including the prevention of oxidative stress, anti-inflammatory ability, mitigation of heart disease risk, and defense against multiple cancer types (Afrin et al. 2016). The nonclimacteric fruits of strawberry have a limited postharvest life because of weight loss (WL), texture softening, quick spoiling, and physiological abnormalities. Even at low temperatures (0 to 2 °C), the storage life of fully ripe strawberry fruits is usually approximately 7 to 10 d in atmospheric air; however, it is highly dependent on the cultivar (John et al. 2024; Kahramanoğlu 2019). Microbial growth and oxidative stress are among the primary factors that contribute to the decline in fruit quality, which occurs in fresh fruits during postharvest storage (John et al. 2024; Kahramanoğlu et al. 2022). Storage at low temperatures helps to increase the storability periods by reducing respiration and transpiration; however, the loss of cell structure reduces fruit quality (Del Olmo et al. 2022). Reactive oxygen species (ROS) cause oxidative damage to cell components and alter the permeability and integrity of cell membranes, which may lead to impaired cell function and cell death and reduce the enzyme activity (Hasanuzzaman et al. 2020). Oxidative stress can also result in turgor loss, a reduction in biological characteristics, and an increase in the vulnerability of tissues to mechanical damage and microbial infections (Zhou et al. 2014). Therefore, several researchers recommend storing strawberries at slightly higher temperatures ranging from 3 to 4 °C (<5 °C) (Kahramanoğlu et al. 2019; Liu et al. 2018) or using protective packaging if stored at temperatures approximately 0 to 2 °C (Ikegaya et al. 2020). However, the advantage gained by reduced oxidative stress at slightly higher temperatures is often lost through increased respiration, transpiration, and pathogen infections (Del Olmo et al. 2022; John et al. 2024).

Various enzymatic [catalase (CAT), ascorbate peroxidase (APX), superoxide dismutase (SOD), and peroxidase (POD)], and nonenzymatic [ascorbic acid (AsA), flavonoids, phenolic acids, and carotenoids] antioxidants comprise the endogenous defense mechanism of plants and fresh fruits against oxidative stress (Gill and Tuteja 2010; Hasanuzzaman et al. 2020). The antioxidant defense mechanism in fruit cells maintain a steady-state balance of ROS while maintaining the ROS at an optimal level can facilitate appropriate redox biology reactions and improve the storability of fruits (Fan et al. 2023; Xu et al. 2021).

Melatonin {C13H16N2O2; IUPAC ID: N-[2-(5-methoxy-1H-indol-3-yl)ethyl]acetamide} is a well-known endogenous indole compound of animals that is also found in different plant parts, including roots, stems, leaves, fruits, and seeds that has several significant physiological functions, including seed germination, rooting, growth, photosynthesis (Arnao and Hernández-Ruiz 2019; Huang et al. 2022), yield improvement (Okatan et al. 2022), protection against abiotic and biotic stresses including drought (Korkmaz et al. 2022), salinity (El-Bauome et al. 2024), and pathogen infections (Shahani et al. 2023). Exogenous applications of melatonin to stored fruits and vegetables also increase antioxidant activity, inhibit browning, delay softening, enhance disease resistance, regulate ripening and senescence, and prolong the storability of fruits and vegetables (Fan et al. 2023; Li et al. 2019; Menaka et al. 2024).

Several studies of different fruits, including guava (Menaka et al. 2024), blackberry (Shah et al. 2023), pomegranate (Molla et al. 2022), and orange (Ma et al. 2021), have been performed, but not much is known about how exogenous melatonin applications affect the fruit quality and postharvest life of strawberry (Liu et al. 2018). Therefore, the current study aimed to evaluate how exogenous melatonin applications affect the postharvest quality and enzymatic activity of strawberry fruits while stored at 4 °C.

Materials and Methods

Materials.

Strawberry fruits (Fragaria ×ananassa cv. Rubygem) used for the present study were hand-collected at commercial maturity from a farm located in Yayla Village, Northern Cyprus, on 5 Feb 2024. Harvested fruits were promptly brought to the horticulture laboratory of the European University of Lefke within 15 min in a protected and ventilated vehicle to maintain harvest quality and prevent losses. Melatonin [N-acetyl-5-methoxytryptamine (C13H16N2O2); CAS number 73-31-4] in powder form (≥98% TLC) was dissolved and according to the methods detailed in this article.

Experimental design, treatments, and storage.

A total of 288 fruits were included in the storage studies performed during this study. The trials were performed with four replicates for three different treatments (control, 200 μM melatonin, and 500 μM melatonin). The respective melatonin doses tested during this study were determined based on the author’s experience and by considering previous studies of strawberry (Liu et al. 2018), ‘Summer Black’ grape (Xia et al. 2021), and litchi (Marak et al. 2023) fruits. Therefore, the fruits that were preselected and allocated for the trials were randomly distributed to three different groups (96 fruits in each group). Then, the fruits in each group (treatment) were again randomly distributed to four different replicates. The storage trials continued for 18 d and at 3-d intervals (3 to 6–9 d to 12–15 to 18 d); four fruits from each replicate (a total of 4 × 4 = 16 for each treatment) were taken out of storage, and the relevant quality parameters were measured.

Fruits of uniform ripeness and size [average weight, 13.9 g; average soluble solids concentration (SSC), 10.2%; average titratable acidity (TA), 0.84 g/100 g citric acid] with no visible disease or mechanical damage were selected for the storage trials. Strawberry fruits were first washed with distilled water and then soaked in 0.02% (weight/volume) sodium hypochlorite solution for 15 s. After the relevant melatonin doses were prepared, the fruits of that dose group were kept in the relevant solution (20 °C) for 5 min. The fruits of the control group were kept in distilled water for the same amount of time. After the treatments, the fruits were dried at room temperature for 2 h until no drops remained on the surface. After drying, the fruits were placed in open polyethylene containers (thickness, 0.03 mm). Four fruits were placed in each container after the initial weights of the fruits were weighed with a digital scale (±0.01 g) and noted. All samples were stored at 4.0 ± 0.5 °C and 90% to 95% relative humidity.

Quality analysis.

During the 18 d of storage, several quality characteristics of the test fruits were regularly measured using 3-d intervals (3 to 6–9 d to 12–15 to 18 d). The methods used to determine the relevant quality analyses are detailed in the following sections.

Weight loss.

The WL of strawberry fruits was calculated by measuring the initial weight and final weight of each fruit at each measurement point, and the results were expressed as the percent change. A digital scale (±0.01 g) was used to determine the fruit weight.

Soluble solids concentration.

The fruits of each replication were manually pressed to extract juice for additional studies. The SSC of each fruit was measured using a hand refractometer (0–32% Brix; Greinorm, Bavaria, Germany) and expressed as the percentage of Brix.

Titratable acidity.

The TA of fruit samples was calculated using the method and formula provided by the AOAC (1990). First, 10 mL of samples was dissolved in 50 mL of distilled water, then the solution was titrated with 0.1 N NaOH until it reached pH 8.1. Furthermore, the TA was determined as g/100 g of citric acid using the following formula:
TA (g/100 g citric acid)=((amount of NaOH (mL)) × 0.006410)×100

Fruit firmness.

The firmness (kg·cm−2) of fruits was measured by a hand penetrometer (GY-1 with a cylindrical probe of Ø3.5 mm). Two distinct locations of each fruit were used to measure fruit firmness. The penetration depth was 10 mm.

Decay incidence.

The severity of decay was assessed by observing the decay area on the fruit surface using the 0 to 5 scale of Liu et al. (2018), where 0 refers to healthy fruits with no decay, 1 refers to 1% to 20% decay on the fruit surface, 2 refers to 21% to 40% decay on the fruit surface, 3 refers to 41% to 60% decay on the fruit surface, 4 refers to 61% to 80% decay on fruit surface, and 5 refers to ≥81% decay on the fruit surface. Then, the decay incidence (the incorporation of both the incidence and severity) was expressed as the weighted means of decay as a percentage of the maximum possible level by following the general formula provided by Feliziani et al. (2015). The formula for the calculation of the decay incidence (%) is as follows:
I=[(d×f)(N×5)]×100

In Eq. [1], “d” is the category of decay severity score, “f” is its frequency, “N” is the total number of sampled fruits, and 5 is the highest category score of decay severity.

Ascorbic acid.

The AsA content (mg/100 g) of the strawberry fruits was determined by following the 2, 6-dichlorophenol indophenol titration method (Jones and Hughes 1983).

Malondialdehyde content.

The method presented by Liu et al. (2018) was used to measure the malondialdehyde (MDA) content. First, a 0.1-g fruit sample was homogenized with 0.9 mL of 10% cold trichloroacetic acid and then incubated in an ice bath for 10 min. Then, 50 μL of the supernatant was combined with 1 mL of 10% trichloroacetic acid-containing 0.67% thiobarbituric acid following centrifugation at 12,000 rpm for 15 min at 4 °C. After 20 min of incubation at 95 °C, the mixture was centrifuged again for 10 min at 4 °C at 12,000 rpm. Then, the absorbance of the final mixture was measured at 450 nm, 532 nm, and 600 nm using ultraviolet/VIS spectrophotometer. Using the following formula, the MDA content was determined and represented as nmol·g−1 of the fruit fresh weight:
MDA (nmol·g1) = 6.45× (OD532OD600)×0.56×OD450

Antioxidant capacity.

The antioxidant capacity [2,2-Di-(4-tert-octylphenyl)-1-picrylhydrazyl (DPPH) scavenging capacity assay] of the strawberry samples during storage was assessed using the method of Liu et al. (2018) with slight modifications. First, 5 mL of strawberry juice was mixed with 5 mL of methyl alcohol (80%) and centrifuged at 4000 rpm for 10 min at 4 °C. Next, the 0.1 mL of supernatant was added to 1 mmol·L−1 DPPH in methanol. After giving the reaction mixture a thorough shake and letting it remain at room temperature for 30 min, the absorbance at 517 nm was measured using the ultraviolet/VIS spectrophotometer. The percent of inhibition of DPPH was calculated as follows:
DPPH scavenging capacity (%)AcAsAc×100

where Ac is the absorbance of the control (without supernatant) and As is the absorbance of the sample.

Antioxidant enzyme activity.

The activities of the antioxidant enzymes (CAT, APX, POD, and SOD) were all assessed by following the methods of Promyou et al. (2023). All enzymes were extracted at 4 °C. Then, 2-g fruit samples were homogenized in 20 mL of 50 mM sodium phosphate buffer (pH 7.8) solution containing 1 mM EDTA, 0.3% (volume/volume) Triton × −100, and 1% (weight/volume) polyvinyl polypyrrolidone for 3 min. After the homogenate was filtered using cheesecloth, the filtrate was centrifuged at 15,000 gn for 20 min at 4 °C.

To determine the CAT activity, 0.1 mL of crude enzyme extract was mixed with 2.9 mL of 25 mM H2O2. Subsequently, using distilled water as the blank, the absorbance of the mixture was measured at 240 nm every 30 s for 3 min. A 0.01 decrease per minute in absorbance at 240 nm was used to define 1 unit of CAT activity, and the data were reported as units per mg protein.
CAT activity (U·mg1 protein) = ΔOD240×V0.01×Δt×Vs×W

In the aforementioned formula, △OD240 is the absorbance change value of reaction mixture; V is the total volume of sample extraction solution (mL); △t is the enzymatic reaction time (min); Vs is the volume of the sample extraction liquid taken during measurement (mL); and W is the sample weight (g).

The reduction in AsA served as a proxy for the APX activity; 0.1 mL of crude enzyme extract was mixed with 0.5 mL of 100 mM potassium phosphate buffer (pH 7.0), 0.5 mL of 1 mM AsA, 0.5 mL of 0.4 mM EDTA, 0.02 mL of 10 mM H2O2, and 0.38 mL of distilled water to obtain the test reaction solution. At 290 nm, the absorbance of the mixture was measured. The activity of an enzyme was measured in units per mg protein, with one unit being the increase in absorbance per minute. The formula for the calculation of APX activity (U·mg−1 protein) was same as that for the CAT activity, except the △OD240 was changed to △OD290 for APX activity.

The capacity to change guaiacol into tetraguaiacol was used to calculate the POD activity; 0.5 mL of crude enzyme extract, 0.5 mL of 2% (volume/volume) H2O2, 1 mL of 50 mM sodium phosphate buffer (pH 5.5), and 1 mL of 25 mM guaiacol comprised the reaction mixture. Using distilled water as the bank, the absorbance was measured at 470 nm every 30 s for 3 min. The amount of enzyme required to produce an absorbance change of 0.01 per minute was considered one unit of POD activity, and the data were represented in units per mg protein. The formula for the calculation of POD activity was, again, the same as that used for the CAT activity, except the △OD240 was changed to △OD470 for POD activity.

The ability of SOD to prevent nitro blue tetrazolium from being reduced photochemically was used to measure its activity. For this purpose, 0.1 mL of the aforementioned extract was mixed with 0.1 mL of 0.6 µM riboflavin, 0.1 mL of 20 µM nitro blue tetrazolium dissolved in 70% ethanol, 0.2 mL of 0.1% (volume/volume) Triton-X, 0.2 mL of 22 µM methionine, 0.5 mL of 50 mM sodium phosphate buffer (pH 5.0), and 0.8 mL of distilled water. Then, the absorbance of the final mixture was measured at 560 nm. One unit of SOD activity was defined as the amount of enzyme that inhibited 50% nitro blue tetrazolium at 560 nm. The total enzyme activity was calculated based on the following formula and expressed as units per mg protein:
SOD activity (U·mg1 protein) (ODCODS)×V0.5×ODC×Vs×W

In the aforementioned formula, ODC is the absorbance value of the reaction mixture in the illumination control tube; ODS is the absorbance value of the reaction mixture in the sample tube; and the other abbreviations are same as those of the CAT formula.

Statistical analysis.

The data for each parameter were first summarized with the help of Microsoft Excel, and figures were created by calculating the mean and SDs (see Supplemental Raw Data S1). Then, a two-way analysis of variance was performed to determine whether there is a statistically significant difference between the treatments, measurement points, and their interactions. Moreover, if a significant difference was detected, then Tukey’s honestly significant difference test was performed at a significance level of P < 0.05 to clarify the difference. All these analyses were performed with the help of the SPSS 22.0 package program. Then, a principal component analysis (PCA) and correlations analysis were performed by using R 4.3.3 software and its free packages. The prcomp() function of “ggfortify” package (Tang et al. 2016) was applied to calculate and visualize the PCA–biplot analysis. Next, the corrplot package (Wei and Simko 2021) was used to compute the correlation among the quality parameters.

Results

Impacts of melatonin on WL, SSC, TA, and AsA.

As presented in Fig. 1A, significant WL of strawberry fruits was determined during the storage period. Because the fruits of the control group were completely rotten on day 18, no measurement and evaluation could be performed. In this case, a very high WL of 10.6% was observed in the control group at the end of day 15. However, as expected, the WL of melatonin-treated fruits was less than that of the control group. The WL of strawberries treated with both melatonin doses was significantly lower than that of the control treatment during the storage period. For the fruits treated with 200 μM melatonin, 9.0% WL was realized at the end of day 18, which was lower than the WL of the control group on day 15. For strawberries treated with 500 μM melatonin, the WL was lower than that of both the control and 200 μM melatonin groups. At the end of day 18, better preservation was achieved than that of the group treated with 500 μM melatonin with 7.2% WL. The current findings highlighted that melatonin treatment protects the postharvest preservation quality of strawberries and delays losses. The 500 μM melatonin application especially kept the WL of strawberries at the lowest level. However, the 200 μM melatonin application was less effective than the 500 μM application, indicating that the impact of melatonin is dose-dependent.

Fig. 1.
Fig. 1.

Impacts of melatonin on the (A) weight loss, (B) soluble solids content (SSC), (C) titratable acidity (TA), and (D) ascorbic acid (AsA) of strawberry fruits during 18 d of storage. The presence of the same lowercase letters next to the mean values of the treatments under the figures indicates that there is no statistically significant difference between the treatments at P ≤ 0.05 according to Tukey’s honestly significant difference (HSD) test.

Citation: HortScience 59, 9; 10.21273/HORTSCI17991-24

An analysis of the SSC content data showed that all fruits exhibited an increase in the SSC content over the course of the storage period following strawberry harvest (Fig. 1B). This increase occurred was faster in the control group than in the groups of melatonin-treated fruits, and the SSC value increased to 13.3% at 15 d after harvest. In the 200 μM melatonin group, the SSC value of strawberries at harvest started at 10.2% and increased throughout the storage period, reaching 13.0% at the end of day 18. In the group treated with 500 μM melatonin, the SSC value increased to 12.6% at the end of day 18. In contrast to the SSC content, the TA values decreased during the storage period, as expected. This value started at 0.84 g/100 g in the control group and decreased to 0.55 g/100 g at the end of day 15. The decrease in TA values of melatonin-treated fruits was realized later than that of the control group, and the value of the control group at day 15 was reached in the melatonin-treated fruits at the end of day 18 (Fig. 1C).

An analysis of the variations in the AsA values over the storage period revealed a consistent increase in the associated values, with the control group experiencing a marginally greater increase in this regard. However, this increase was not statistically significant (P < 0.05). The AsA level increased in the control group from 31.5 mg/100 g to 56.5 mg/100 g over the course of the storage period following strawberry harvest. Similarly, fruits treated with 200 μM and 500 μM melatonin also showed an increase; at the end of the storage period, the average AsA values of the fruits in both treatment groups were 59.7 mg/100 g and 60.7 mg/100 g, respectively. An additional sign of improved antioxidant capability is increased AsA.

Impact of melatonin on fruit firmness and decay incidence.

The firmness of strawberry fruits in all treatments showed a downward trend over the postharvest storage period (Fig. 2A). After being 0.91 kg·cm−2 at harvest, the firmness value decreased throughout storage; at the end of the 15-d period, it was only 0.45 kg·cm−2 in the control group. Conversely, after 18 d, the firmness value of the strawberries in the group that received 200 μM melatonin decreased to 0.45 kg·cm−2. The group treated with 500 μM melatonin had a firmness value of 0.49 kg·cm−2 on the same date. The results indicated that melatonin treatments at 200 μM and 500 μM were only partially successful at preserving the firmness of the strawberry fruits. In contrast to the control group, it was shown that melatonin treatments were unable to fully stop the loss of firmness; by the end of day 18, the firmness of the fruit flesh had decreased.

Fig. 2.
Fig. 2.

Impacts of melatonin treatment on the (A) fruit firmness and (B) decay incidence of strawberry fruits during 18 d of storage. The presence of the same lowercase letters next to the mean values of the treatments under the figures indicates that there is no statistically significant difference between the treatments at P ≤ 0.05 according to Tukey’s honestly significant difference (HSD) test.

Citation: HortScience 59, 9; 10.21273/HORTSCI17991-24

Decay of the control group was first observed after 3 d of storage, whereas the first symptoms of decay of the 200 μM melatonin group were observed after 9 d, and those of the 500 μM melatonin group were observed after 12 d (Fig. 2B). Hereafter, the decay incidence increased as the storage time progressed. However, this increase occurred very quickly in the control group, whereas it was delayed and prevented with melatonin treatment. The average decay incidence of the control group was 72.5% at 15 d of storage, and it 100.0% at 18 d. However, 500 μM melatonin very effectively prevented the decay incidence; the decay incidence of strawberry fruits treated with 500 μM melatonin was only 28.8% after 18 d of storage.

Impact of melatonin on the MDA content and antioxidant activity.

In the current study, melatonin treatment had a considerable negative impact on the MDA contents of strawberry fruits, which had greatly increased during storage. The current research suggested that applying melatonin to strawberry fruit could improve its resistance to oxidative stress induced by senescence and postpone fruit senescence (Fig. 3A). The results showed that strawberries treated with 200 μM and 500 μM melatonin had reduced MDA levels. The MDA levels of the control group increased over the course of the storage period, peaking at 66.1 nmol·g−1 by the end of day 15. Nonetheless, the MDA levels of the fruits treated with 500 μM melatonin increased, but the increase was less than that of fruits treated with 200 μM melatonin and that of the control group. In particular, 500 μM melatonin dramatically reduced MDA levels compared with those of the control group.

Fig. 3.
Fig. 3.

Impacts of melatonin treatment on the (A) malondialdehyde (MDA) content and (B) 2,2-diphenyl-1-picrylhydrazyl (DPPH) scavenging capacity of strawberry fruits during 18 d of storage. The presence of the same lowercase letters next to the mean values of the treatments under the figures indicates that there is no statistically significant difference between the treatments at P ≤ 0.05 according to Tukey’s honestly significant difference (HSD) test.

Citation: HortScience 59, 9; 10.21273/HORTSCI17991-24

The DPPH (2,2-diphenyl-1-picrylhydrazyl) radical scavenging activity is a common method used to measure the antioxidant capacity of a substance. Higher DPPH scavenging activity means higher antioxidant capacity. The impact of melatonin on the antioxidant capacity of strawberry fruits was also tested during the current study. The DPPH scavenging capacity was used for this purpose. According to the results of this study, the DPPH radical scavenging activity increased during the storage period; however, as expected, this increase was higher in melatonin-treated strawberry fruits compared with that of the control group (Fig. 3B). With both treatments, the DPPH radical scavenging activity was measured as 82.2% at harvest time, and this value increased to 89.1% in the control group at the end of day 15. With the 200 μM melatonin application, the DPPH radical scavenging activity increased to 94.2% at the end of day 18, whereas the 500 μM melatonin application provided a similar impact on DPPH radical scavenging activity, which increased to 94.0% on the same date. No significant difference was observed between the melatonin treatments. These findings support that melatonin can increase the antioxidant capacity of strawberries.

Impact of melatonin on enzymatic activities.

The effects of 200 μM and 500 μM melatonin on the enzyme activities of strawberry fruits are shown in Fig. 4A–D. The key antioxidant enzymes of ROS scavenging are CAT, APX, POD, and SOD (Mittler 2002). One of the most important results of this study was that the melatonin treatments (both 200 μM and 500 μM) effectively increased the CAT enzyme activity in strawberries. Accordingly, in the control group, the CAT enzyme activity, which was 6.4 U·mg−1 at harvest, increased to 7.7 U·mg−1 at the end of day 6, but this value decreased to 5.8 U·mg−1 at the end of day 15. However, with 200 μM melatonin, the CAT enzyme activity showed a significant increase during the storage period and increased to 12.8 U·mg−1 on day 9; however, it then decreased to 10.0 U·mg−1 at the end of day 18. Similarly, with 500 μM melatonin, the CAT enzyme activity increased and then decreased during the preservation period; it was 10.2 U·mg−1 at the end of day 18. The CAT enzyme activity at the end of the storage period was significantly higher than the initial value measured at harvest and the value of the control group.

Fig. 4.
Fig. 4.

Impacts of melatonin treatment on the (A) catalase (CAT), (B) ascorbate peroxidase (APX), (C) peroxidase (POD), and (D) superoxide dismutase (SOD) enzymatic activities of strawberry fruits during 18 d of storage. The presence of the same lowercase letters next to the mean values of the treatments under the figures indicates that there is no statistically significant difference between the treatments at P ≤ 0.05 according to Tukey’s honestly significant difference (HSD) test.

Citation: HortScience 59, 9; 10.21273/HORTSCI17991-24

Based on the findings obtained during this study, melatonin treatments (both 200 μM and 500 μM) effectively increased the APX enzyme activity in strawberries. As in the case of CAT enzymes, this increase showed a significant difference compared with that of the control and showed a relative increase during the first 9 d and then entered a downward trend; however, this decreased value remained higher than the initial value (Fig. 4B).

Similar to the CAT and APX enzymes, the POD activity in strawberry fruits also showed an increase during the storage period, and this increase was significantly triggered by melatonin applications. The POD enzyme activity of the control group, which was 10.4 U·mg−1 at harvest, increased to 14.1 U·mg−1 at the end of day 15 (Fig. 4C). However, the POD enzyme activity values of the fruits treated with 200 μM and 500 μM melatonin on the same date were 29.1 U·mg−1 and 31.6 U·mg−1, respectively, which were more than twice that of the control. After this date, a decrease was observed in the POD enzyme activity of melatonin-treated fruits.

During this study, melatonin treatments (both 200 μM and 500 μM) effectively increased the SOD enzyme activity in strawberries (Fig. 4D). The SOD enzyme activity of the control group, which was 0.6 U·mg−1 at harvest time, increased to 1.4 U·mg−1 at the end of day 15. However, the SOD enzyme activity increased to 1.9 U·mg−1 at the end of day 15 with 200 μM melatonin, and to 1.9 U·mg−1 with 500 μM melatonin. Therefore, melatonin may increase the antioxidant capacity of strawberries and may effectively manage oxidative stress.

Correlation and PCA–biplot analysis results.

The results of the correlation analysis performed to examine the relationship between the quality parameters of strawberry fruits are presented in Fig. 5A. According to these results, the highest positive correlation was found between MDA and DI (0.93), followed by the correlation between MDA and WL (0.92), indicating that these three important indicators of quality loss in strawberries act together. Similarly, high positive correlations were found between DI and WL, APX and CAT, DPPH and AsA, and AsA and MDA. The highest negative correlation was −0.77 between MDA and firmness. Similarly, firmness showed a high negative correlation with WL, DI, and AsA. Similar to firmness, TA also showed a high negative correlation with the same parameters. However, it was observed that APX and CAT enzymes were the most important parameters that negatively affected DI, MDA, and WL, which are the most important indicators of quality loss of fruits, whereas the effects of SOD and POD enzymes were less significant.

Fig. 5.
Fig. 5.

Results of the correlation analysis (A) and principal component analysis (PCA)–biplot analysis (B).

Citation: HortScience 59, 9; 10.21273/HORTSCI17991-24

A PCA was conducted according to the correlation matrix because of the high correlation among the quality parameters. An examination of the ratios of the eigenvalues that explained the total variance showed that the first dimension (principal component) alone explained 49.3% of the total variance, whereas the second dimension explained 32.5% of the total variance. The first two principal components together explained 81.8% of the variance (Fig. 5B). A graphical explanation of the results showed that, as expected, the individuals that belong to the control treatment formed a separate group, and that the two different doses of melatonin formed different groups close to each other. The consistency of our results was demonstrated by the variables that were close to the control treatment, i.e., WL, MDA, and DI, which are signs of fruit spoilage. However, the distribution of variables around the principal components showed that MDA, WL, DI, AsA, firmness, TA, and SSC were concentrated around the first component, whereas POD, SOD, CAT, DPPH, and APX were concentrated around the second component (Fig. 5B and Table 1). An examination of the impact of melatonin doses on the variables of the second component made it possible to conclude that the application of 500 µM melatonin had a greater effect, especially on the enzyme activities.

Table 1.

PCA results of the variables (parameters).

Table 1.

Discussion

Microbial decay, WL, and oxidative stress are the main causes of fruit quality decline during storage (John et al. 2024; Kahramanoğlu et al. 2022). The results of the present study also confirmed this information, whereas the three quality parameters (WL, DI, and MDA) of the control group were high and had a high correlation, as explained by PCA. Low temperature storage lengthens the periods of storability, but the quality is decreased because of cell structure breakdown (Del Olmo et al. 2022). The findings of the present research demonstrated that the exogenous melatonin application reduced the WL of the stored strawberry fruits. This reduction was dose-dependent, and the 500-μM melatonin dose provided better results than the 200-μM melatonin dose. Several studies found that melatonin increases the stress tolerance of plant tissues and may improve postharvest preservation quality (Arnao and Hernández-Ruiz 2015; Tan et al. 2012). The results of the current study are similar to those of Liu et al. (2018), whose study of strawberries was important and similar to ours. Moreover, the success of melatonin in preventing WL has been previously proven for various fruits, such as peaches (Gao et al. 2016), apples (Onik et al. 2021), ‘Newhall’ navel orange (Ma et al. 2021), and cattails (Fan et al. 2023).

Furthermore, WL alone is not sufficient for determining quality. Additionally, measurements of SSC and TA, which have direct effects on the fruit flavor, showed a significant increase in the SSC and a decrease in the TA during the storage period. Melatonin delayed the changes in both quality parameters and slowed fruit senescence. Some studies of the effects of melatonin on plant metabolism appear in the literature. Melatonin can delay not only the WL observed during senescence but also the changes in SSC and TA (Ma et al. 2021).

One of the most significant components of the nutritional quality of strawberry fruits is AsA (Davey et al. 2000). The current results also showed that the melatonin application significantly delayed the changes in AsA. An additional sign of improved antioxidant capability is elevated AsA. Not surprisingly, the APX activity and antioxidant activity of the melatonin-treated fruits were higher than those of the control group. The positive impact of melatonin on the AsA of the fruits was previously noted by Liu et al. (2018), and the current results are in accordance with those findings.

Fruit firmness is a crucial determinant of fruit quality during postharvest storage (Liu et al. 2019). It is well-known to be affected by the cell wall structure (Liu et al. 2019). In current study, fruit firmness showed a decreasing trend over the postharvest storage period, but the melatonin application was found to delay this decrease. Melatonin can delay the decrease in fruit firmness by altering the metabolism of plant cell wall components. The findings of the current study are in accordance with those of several other studies that noted similar impacts of melatonin on fruit firmness (Liu et al. 2018; Tan et al. 2020).

Melatonin application also significantly reduced the microbial decay in strawberry fruits during storage. The ability of melatonin to prevent fruit decay could be linked to increased fruit resistance to disease (Li et al. 2019) and can be explained by the reduced MDA content and increased enzymatic activities (Fan et al. 2023; Li et al. 2019; Menaka et al. 2024; Tan et al. 2020). Fruit senescence is primarily caused by oxidative stress and ROS build-up. Because of its long half-life in cells, hydrogen peroxide (H2O2) is the primary ROS that causes damage. Low doses of H2O2 modulate plant development as a secondary messenger; nevertheless, high doses of H2O2 cause oxidative stress burst and lipid peroxidation (Onik et al. 2021). In this case, the result of this oxidation reaction is MDA, and the amount of MDA indicates the extent of oxidative damage (Diao et al. 2022). In the present study, melatonin treatment had a considerable negative impact on the MDA contents of strawberry fruits, which had also greatly increased during storage. These results lend credence to the idea that the cellular integrity and postharvest life span of strawberry fruits may be safeguarded by melatonin treatment. Similar studies of the restricted peroxidation of membrane lipids resulting from melatonin applications during the postharvest storage of apples (Onik et al. 2021), cattails (Fan et al. 2023), and litchi (Zhang et al. 2018) have been conducted. In this study, the melatonin application increased the antioxidant capacity of strawberries. Additionally, melatonin can increase DPPH radical scavenging activity because of its antioxidant properties (Liu et al. 2018), and the current results support those reported in the literature.

Fruit senescence is the result of respiration and ROS generation postharvest (John et al. 2024). Additionally, CAT, APX, POD, and SOD are the key antioxidant enzymes of ROS scavenging (Mittler 2002). Furthermore, CAT is responsible for the breakdown of H2O2 (catalyzes the decomposition of H2O2 into H2O and O2) in cells, and it is an important part of the antioxidant defense system. An increase in enzyme activity indicates that cells produce more CAT to cope with oxidative stress (Ge et al. 2024). APX is also responsible for the reduction of H2O2 with AsA in cells and plays an important role in the neutralization of oxidative stress (Ge et al. 2024). Furthermore, POD can slow the senescence of harvested fruits and scavenge free radicals (Fan et al. 2023). Although CAT and POD are the main enzymes that break down H2O2, SOD can shield cells from oxidative damage (Mittler 2002). Furthermore, SOD is an enzyme responsible for the detoxification of superoxide radical (O2.-) in cells.

These results suggested that the application of melatonin could be responsible for reducing the ROS level and improving the storage quality of strawberry fruits. The findings of the present study are in agreement with those of the studies by Gao et al. (2016) (peach), Zhang et al. (2018) (litchi), Onik et al. (2021) (apples), and Fan et al. (2023) (cattails). The results of this study are also in agreement with the results of two other studies of chitosan (Bahmani et al. 2022) and melatonin (Promyou et al. 2023) in strawberry fruits. Although several differences were observed, the findings indicated that melatonin treatment, like chitosan, improves the postharvest preservation quality of strawberry fruits by increasing enzyme activity.

Conclusions

This research provided insights regarding how melatonin prevents the deterioration of strawberry fruits during storage by improving enzyme activity. Exogenous melatonin significantly increased the activity of antioxidant enzymes, including CAT, APX, SOD, and POD, at the physiological level, resulting in a reduction in WL, the decay incidence, and the MDA level, as well as delayed changes in SSC, TA, AsA, and fruit firmness. The evidence in the literature and the results of this study indicated that 500 µM melatonin has the potential to prolong the storability of strawberry fruits. However, additional information regarding various strawberry cultivars and harvest maturity stages is necessary to guarantee the greatest benefits from melatonin at the lowest dosage.

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  • Fig. 1.

    Impacts of melatonin on the (A) weight loss, (B) soluble solids content (SSC), (C) titratable acidity (TA), and (D) ascorbic acid (AsA) of strawberry fruits during 18 d of storage. The presence of the same lowercase letters next to the mean values of the treatments under the figures indicates that there is no statistically significant difference between the treatments at P ≤ 0.05 according to Tukey’s honestly significant difference (HSD) test.

  • Fig. 2.

    Impacts of melatonin treatment on the (A) fruit firmness and (B) decay incidence of strawberry fruits during 18 d of storage. The presence of the same lowercase letters next to the mean values of the treatments under the figures indicates that there is no statistically significant difference between the treatments at P ≤ 0.05 according to Tukey’s honestly significant difference (HSD) test.

  • Fig. 3.

    Impacts of melatonin treatment on the (A) malondialdehyde (MDA) content and (B) 2,2-diphenyl-1-picrylhydrazyl (DPPH) scavenging capacity of strawberry fruits during 18 d of storage. The presence of the same lowercase letters next to the mean values of the treatments under the figures indicates that there is no statistically significant difference between the treatments at P ≤ 0.05 according to Tukey’s honestly significant difference (HSD) test.

  • Fig. 4.

    Impacts of melatonin treatment on the (A) catalase (CAT), (B) ascorbate peroxidase (APX), (C) peroxidase (POD), and (D) superoxide dismutase (SOD) enzymatic activities of strawberry fruits during 18 d of storage. The presence of the same lowercase letters next to the mean values of the treatments under the figures indicates that there is no statistically significant difference between the treatments at P ≤ 0.05 according to Tukey’s honestly significant difference (HSD) test.

  • Fig. 5.

    Results of the correlation analysis (A) and principal component analysis (PCA)–biplot analysis (B).

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    • Export Citation
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    • Search Google Scholar
    • Export Citation
  • Bahmani R, Razavi F, Mortazavi SN, Gohari G, Juárez-Maldonado A. 2022. Evaluation of proline-coated chitosan nanoparticles on decay control and quality preservation of strawberry fruit (cv. Camarosa) during cold storage. Horticulturae. 8(7):648. https://doi.org/10.3390/horticulturae8070648.

    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
  • Del Olmo I, Romero I, Alvarez MD, Tarradas R, Sanchez-Ballesta MT, Escribano MI, Merodio C. 2022. Transcriptomic analysis of CO2-treated strawberries (Fragaria vesca) with enhanced resistance to softening and oxidative stress at consumption. Front Plant Sci. 13:983976. https://doi.org/10.3389/fpls.2022.983976.

    • Search Google Scholar
    • Export Citation
  • Diao QN, Cao YY, Wang H, Zhang YP, Shen HB. 2022. Nitric oxide confers chilling stress tolerance by regulating carbohydrate metabolism and the antioxidant defense system in melon (Cucumis melo L.) seedlings. HortScience. 57(10):12491256. https://doi.org/10.21273/HORTSCI16677-22.

    • Search Google Scholar
    • Export Citation
  • El-Bauome HA, Doklega SM, Saleh SA, Mohamed AS, Suliman AA, Abd El-Hady MA. 2024. Effects of melatonin on lettuce plant growth, antioxidant enzymes and photosynthetic pigments under salinity stress conditions. Folia Hortic. 36(1):117. https://doi.org/10.2478/fhort-2024-0001.

    • Search Google Scholar
    • Export Citation
  • Fan A, Wan C, Liu H, Xiong X, Nong Y, Kahramanoğlu İ, Yang R, Zeng L. 2023. Melatonin treatment maintains the quality and delays senescence of postharvest cattails (Typha latifolia L.) during cold storage. Food Chem X. 19:100796. https://doi.org/10.1016/j.fochx.2023.100796.

    • Search Google Scholar
    • Export Citation
  • Feliziani E, Landi L, Romanazzi G. 2015. Preharvest treatments with chitosan and other alternatives to conventional fungicides to control postharvest decay of strawberry. Carbohydr Polym. 132:111117. https://doi.org/10.1016/j.carbpol.2015.05.078.

    • Search Google Scholar
    • Export Citation
  • Gao H, Zhang ZK, Chai HK, Cheng N, Yang Y, Wang DN, Yang T, Cao W. 2016. Melatonin treatment delays postharvest senescence and regulates reactive oxygen species metabolism in peach fruit. Postharvest Biol Technol. 118:103110. https://doi.org/10.1016/j.postharvbio.2016.03.006.

    • Search Google Scholar
    • Export Citation
  • Ge Q, Zhao S, Shao X, Wei Y, Chen J, Wang H, Xu F. 2024. Transcriptomic analysis reveals the resistance mechanism of flavonoids from Sedum aizoon L. to Rhizopus nigricans in postharvest strawberry fruit. Postharvest Biol Technol. 209:112723. https://doi.org/10.1016/j.postharvbio.2023.112723.

    • Search Google Scholar
    • Export Citation
  • Gill SS, Tuteja N. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem. 48(12):909930. https://doi.org/10.1016/j.plaphy.2010.08.016.

    • Search Google Scholar
    • Export Citation
  • Hasanuzzaman M, Bhuyan MB, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA, Fujita M, Fotopoulos V. 2020. Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator. Antioxidants. 9(8):681. https://doi.org/10.3390/antiox9080681.

    • Search Google Scholar
    • Export Citation
  • Huang W, Huang X, Fang Z. 2022. Melatonin-induced rhizome proliferation, differentiation, and rooting during rapid propagation of Cymbidium goeringii and Cymbidium faberi. HortScience. 57(9):10721077. https://doi.org/10.21273/HORTSCI16704-22.

    • Search Google Scholar
    • Export Citation
  • Ikegaya A, Ohba S, Nakajima T, Toyoizumi T, Ito S, Arai E. 2020. Practical long‐term storage of strawberries in refrigerated containers at ice temperature. Food Sci Nutr. 8(9):51385148. https://doi.org/10.1002/fsn3.1817.

    • Search Google Scholar
    • Export Citation
  • John A, Isaac WA, Daley O, Kahramanoğlu İ. 2024. Biological and environmental factors affecting postharvest quality of fruits and vegetables, p 36–64. In: Kahramanoğlu Í (ed). Postharvest physiology and handling of horticultural crops. CRC Press. https://doi.org/10.1201/9781003452355.

    • Search Google Scholar
    • Export Citation
  • Jones E, Hughes RE. 1983. Foliar ascorbic acid in some angiosperms. Phytochemistry. 22(11):24932499. https://doi.org/10.1016/0031-9422(83)80147-2.

    • Search Google Scholar
    • Export Citation
  • Kahramanoğlu İ. 2019. Effects of lemongrass oil application and modified atmosphere packaging on the postharvest life and quality of strawberry fruits. Sci Hortic. 256:108527. https://doi.org/10.1016/j.scienta.2019.05.054.

    • Search Google Scholar
    • Export Citation
  • Kahramanoğlu İ, Panfilova O, Kesimci TG, Bozhüyük AU, Gürbüz R, Alptekin H. 2022. Control of postharvest gray mold at strawberry fruits caused by Botrytis cinerea and improving fruit storability through Origanum onites L. and Ziziphora clinopodioides L. volatile essential oils. Agronomy. 12(2):389. https://doi.org/10.3390/agronomy12020389.

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Supplementary Materials

İbrahim Kahramanoğlu Department of Horticulture, Faculty of Agricultural Sciences and Technologies, European University of Lefke, Northern Cyprus, via Mersin 10 Turkey, 99780

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Contributor Notes

This research was supported by the project grant of the European University of Lefke (grant no. BABKO.0312420).

İ.K. is the corresponding author. E-mail: ibrahimcy84@yahoo.com or ikahramanoglu@eul.edu.tr.

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  • Fig. 1.

    Impacts of melatonin on the (A) weight loss, (B) soluble solids content (SSC), (C) titratable acidity (TA), and (D) ascorbic acid (AsA) of strawberry fruits during 18 d of storage. The presence of the same lowercase letters next to the mean values of the treatments under the figures indicates that there is no statistically significant difference between the treatments at P ≤ 0.05 according to Tukey’s honestly significant difference (HSD) test.

  • Fig. 2.

    Impacts of melatonin treatment on the (A) fruit firmness and (B) decay incidence of strawberry fruits during 18 d of storage. The presence of the same lowercase letters next to the mean values of the treatments under the figures indicates that there is no statistically significant difference between the treatments at P ≤ 0.05 according to Tukey’s honestly significant difference (HSD) test.

  • Fig. 3.

    Impacts of melatonin treatment on the (A) malondialdehyde (MDA) content and (B) 2,2-diphenyl-1-picrylhydrazyl (DPPH) scavenging capacity of strawberry fruits during 18 d of storage. The presence of the same lowercase letters next to the mean values of the treatments under the figures indicates that there is no statistically significant difference between the treatments at P ≤ 0.05 according to Tukey’s honestly significant difference (HSD) test.

  • Fig. 4.

    Impacts of melatonin treatment on the (A) catalase (CAT), (B) ascorbate peroxidase (APX), (C) peroxidase (POD), and (D) superoxide dismutase (SOD) enzymatic activities of strawberry fruits during 18 d of storage. The presence of the same lowercase letters next to the mean values of the treatments under the figures indicates that there is no statistically significant difference between the treatments at P ≤ 0.05 according to Tukey’s honestly significant difference (HSD) test.

  • Fig. 5.

    Results of the correlation analysis (A) and principal component analysis (PCA)–biplot analysis (B).

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