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Communication

Metabolomics Reveals Specific Metabolic Changes in Sweet Cherries (Prunus avium L.) Subjected to Postharvest Treatment with Melatonin after Mechanical Stress

by
Ignacia Hernández
1,
Excequel Ponce
1,
Juan Vidal
1,
Rosana Chirinos
2,
David Campos
2,
Romina Pedreschi
1,3 and
Claudia Fuentealba
1,*
1
Facultad de Ciencias Agronómicas y de los Alimentos, Escuela de Agronomía, Pontificia Universidad Católica de Valparaíso, Calle San Francisco s/n, La Palma, Quillota 2260000, Chile
2
Instituto de Biotecnología (IBT), Universidad Nacional Agraria La Molina—UNALM, Avenida La Molina s/n, Lima 150114, Peru
3
Millennium Institute Center for Genome Regulation, Santiago 8320000, Chile
*
Author to whom correspondence should be addressed.
Horticulturae 2023, 9(8), 940; https://doi.org/10.3390/horticulturae9080940
Submission received: 12 June 2023 / Revised: 25 July 2023 / Accepted: 14 August 2023 / Published: 18 August 2023
(This article belongs to the Special Issue Postharvest Physiology, Biochemistry and Sustainable Management of Plant Genetic Resources)
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Abstract

:
Sweet cherry may develop surface pitting during prolonged cold storage, and susceptibility among varieties is related to metabolites in response to cold and mechanical damage. This study aimed to evaluate the metabolic changes in sweet cherry fruits subjected to melatonin treatment and induced surface pitting. Melatonin (400 µM) was applied to sweet cherries before pitting induction and then stored at 1 °C for 20 d. Melatonin treatment attenuated the severity of pitting damage during cold storage, with an average severity value of 3.1 for cherries with melatonin and 2.6 without melatonin. In addition, melatonin application appeared to modulate metabolic responses due to the regulation of metabolic pathways related to abiotic stress. Upregulation of different secondary metabolites was observed after 16 h of melatonin treatment and cold storage. Moreover, some metabolites of the sphingolipid and sulfur metabolism were upregulated after 10 d. This research is the first to show that melatonin may influence the response of sweet cherries to cold and mechanical damage.

1. Introduction

Chile is geographically distant from its primary sweet cherry export market, specifically China. This situation implies considerable difficulties in successfully delivering high-quality fruits to distant destinations. Sweet cherry can cause significant problems, such as color loss, flavor, firmness, pitting, and pedicel browning during prolonged storage [1]. According to Valenzuela [2], the most prevalent types of damage in sweet cherries are surface pitting and bruising, accounting for 28.9% of the total damage to fruit at the export destination. Loss of firmness is the next most common issue, making up 10.5% of the damage, followed by fruit splitting at 2.4%. Although several recent studies have used image processing as a fast and economical alternative to segregate cherries and/or pits of different cultivars according to texture and color parameters [3,4,5], it is difficult to use these technologies for the early detection of damage or defects that appear during cold storage (more than one week after harvest), such as surface pitting. Low-temperature storage is necessary to preserve the quality attributes of various fruits; however, fruits might develop symptoms of chilling injury, leading to oxidative damage and lipid peroxidation. It has been observed that sweet cherries show a higher incidence of pitting damage after prolonged storage at 1 °C [6]. This defect has been considered one of the main physiological disorders in sweet cherry and is described as indentations (4 to 8 mm) on the surface of the fruits that appear some days after compression is applied [7].
Recently, Fuentealba et al. [8] and Ponce et al. [9] found differences in the level of primary and secondary metabolites between contrasting varieties when subjected to mechanical damage and observed that the variety susceptible to surface pitting presented higher contents of p-coumaric acid derivatives, L-5-oxyproline, D-galactose, and D-galacturonic acid, along with higher solubilization of cell wall pectins. On the other hand, the resistant variety presented higher contents of cell wall material, which might be related to an increase in xyloglucan content after mechanical damage. To understand this physiological problem, several researchers have evaluated different treatments to control the disorder, such as CaCl2, gibberellic acid, hydrogen sulfide, and UV-C light exposure [10,11]. While these applications have had some effect in reducing pitting, the primary metabolism of sweet cherry fruit was altered, impairing quality characteristics such as delayed ripening and sugar and acid contents. Moreover, conventional postharvest technologies, such as 1-methylcyclopropene and modified atmosphere packaging, have not been able to reduce pitting incidence in sweet cherry fruits during cold storage [12].
Cold is used to delay the ripening and aging of fruits, but Zhou et al. [13] reported that activation of certain metabolic responses may collectively contribute to the increased incidence of pitting in blueberries caused by cold damage. Nevertheless, melatonin treatment has been shown to delay sweet cherry ripening and senescence, improving resistance to some diseases and cold tolerance [14]. The success of postharvest treatment with melatonin in sweet cherry is due to its ability to reduce the respiration rate and enhance the antioxidant enzyme system, including superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD), causing a reduction in hydrogen peroxide (H2O2) and malondialdehyde (MDA) [15,16]. In addition, Xia et al. [17] and Bal et al. [18] reported that postharvest melatonin treatments increase the total phenolic, total anthocyanin, and antioxidant content of sweet cherries, which has also been observed with preharvest application during fruit development [19]. To the best of our knowledge, the effect of melatonin treatment on the incidence of mechanical stress, such as surface pitting, in sweet cherries has not yet been reported.
Previous studies have shown that susceptibility to pitting among sweet cherry varieties differs at the metabolite level in response to cold and mechanical damage [8,9]. Therefore, our hypothesis suggests that postharvest treatments with melatonin affect on metabolic pathways related to abiotic stress. The aim of this research is to evaluate the biochemical responses at the metabolite level (primary and secondary) of sweet cherry var. Lapins with induced pitting after postharvest treatment with melatonin and subjected to cold storage.

2. Materials and Methods

2.1. Plant Material

A total of 900 sweet cherry (Prunus avium L.) fruits obtained from four trees (var. Lapins) were harvested with pedicels from an orchard located at the experimental station of the Pontificia Universidad Católica de Valparaíso, located in the city of Quillota, V Region of Valparaíso, Chile (32°53′35″ S, 71°12′31″ W), in November 2022. The crops were grown under standard market conditions.

2.2. Treatment with Melatonin

Melatonin treatment was performed according to the method described by Wang et al. [20], with modifications. Briefly, two groups of 450 fruits each were formed: one group was exposed to melatonin treatment, and the other control group was exposed to distilled water. Immediately after harvesting, 400 µM melatonin solution (or distilled water for control) was sprayed homogeneously on the fruits. For both groups, the fruits were left to dry at room temperature for 1 h. Subsequently, all fruits were stored at 1 °C and 95% relative humidity (RH) for 16 h.

2.3. Induction of Pitting Damage

After melatonin treatment and short cold storage (16 h), pitting damage was induced in each fruit as described by Ponce et al. [9], using a TA-XT2 texture analyzer (Stable Micro Systems Ltd., Godalming, UK). Immediately after damage, the fruits were stored at 1 °C and 95% RH, and the samples were taken at 0 d, 10 d, and 20 d. The samples were placed into plastic clamshells with 50 fruits in each, and each clamshell corresponded to one biological replicate. For each storage time (n = 3), the damage was assessed using a visual scale (from 0 = no pitting to 4 = very severe pitting, Figure S1). Then, the fruits were crushed with liquid nitrogen using an IKA® Basic Analytical Mill A11 (IKA. Staufen, Breisgau, Germany) and stored at −80 °C.

2.4. Targeted and Untargeted Metabolomic Analyses

Extraction and derivatization of polar metabolites were performed according to the method described by Fuentealba et al. [21] using an Agilent 7890B gas chromatograph equipped with a 5977A single quadrupole mass detector and electron impact ionization source (GC–MS) and an HP-5 ms Ultra Inert column (30 m × 0.25 mm × 0.25 µm) (Agilent Technologies, Santa Clara, CA, USA). Chromatographic peaks were deconvoluted and identified by comparing retention times and mass spectra with a library constructed from commercial standards and the NIST14 library using the Mass Hunter Quantitative software (Agilent Technologies, Santa Clara, CA, USA). The data were expressed as relative abundance. Quantification of anthocyanins and phenolic acids was performed as described by Fuentealba et al. [8] using a UPLC-PDA system (Waters, Milford, MA, USA) equipped with an autoinjector, an Acquity BEH C18 column (1.7 μm; 100 × 2.1 mm), Acquity VandGuard BEH C18 precolumn (1.7 μm; 5 × 2.1 mm), and Empower software (Waters, Milford, MA, USA). The phenolic compounds and anthocyanins were identified by comparing their retention times and UV-visible spectra with those of commercial standards. The results were expressed in mg g −1 of the freeze-dried sample.

2.5. Statistical Analysis

Metabolomics data and correlation of response variables were analyzed via principal component analysis (PCA) and partial least squares discriminant analysis (PLS-DA) using MetaboAnalyst 5.0 (https://www.metaboanalyst.ca, accessed on 14 March 2023). Metabolites were associated with the metabolic pathways using MetaboAnalyst 5.0. The criteria were p value < 0.05 and FDR value < 0.5. To evaluate the severity of pitting damage, the data were subjected to multiway analysis of variance (ANOVA) with Tukey’s test for multiple comparisons (p < 0.05) using GraphPad Prism 9 (GraphPad Software Inc., Boston, MA, USA, 2023). The results were expressed as means ± standard deviation.

3. Results

3.1. Severity of Pitting Damage

The samples of the sweet cherry var. Lapins with and without melatonin treatment were analyzed by means of two-way ANOVA. Although there were no significant differences in pitting damage between the treatments on day 20 of cold storage, when comparing days 10 and 20, it was observed that the melatonin treatment did not have a significant increase in severity as was observed in the control group (Figure 1).

3.2. Metabolic Changes after Melatonin Treatment and Pitting Damage

For the metabolomic analysis, PCA and PLS-DA were performed (Figure 2). Treatments and cold storage time were used as categorical variables, and the relative abundance of untargeted metabolites and secondary metabolite concentrations were used as response variables (Table S1). Two PCs were extracted, with no clear separation between the categorical variables (31.5% of the variance explained). In addition, PLS-DA showed a slight separation between the melatonin treatment and the control.
Furthermore, the analysis of metabolomics revealed essential metabolites linked to various metabolic pathways, including phenylpropanoid biosynthesis, stilbenoid biosynthesis, diarylheptanoids and gingerol, flavonoid biosynthesis, anthocyanin biosynthesis, sphingolipid metabolism, sulfur metabolism, and amino sugar and nucleotide sugar metabolism. The metabolites of these pathways exhibited varying degrees of significance, as indicated by their respective p values (<0.05), as shown in Figure 3. This allowed us to clarify the important differences in the regulatory trend (upregulation or downregulation) between melatonin-treated and untreated sweet cherries (Figure 4 and Table S2).

4. Discussion

4.1. Severity of Pitting Damage

Prolonged cold storage of sweet cherry increased the severity of pitting damage in both the melatonin-treated and control fruits, which agrees with previous investigations [6,9]. Melatonin was able to attenuate the severity of pitting damage, which could be related to the defense response against abiotic stress [14]. This first approach to reducing the severity of pitting may serve as the basis for future work to evaluate the effect of melatonin through a dose-dependent study and/or testing a longer cold storage period in which the incidence of temperature is stronger on pitting.

4.2. Metabolic Changes after Melatonin Treatment and Pitting Damage

Cherries are considered very healthy fruits due to their high content of several phenolic compounds, such as anthocyanins, flavonoids, and hydroxycinnamic acids [22]. The phenylpropanoid pathway is very relevant for cherries since it is through this pathway that flavonoids, which are involved in different biological functions, such as resistance to ultraviolet (UV) radiation against pathogen infection and improving postharvest quality of the fruit, are synthesized [23]. Our results showed higher contents of p-coumaroyl quinic acid (which participates in phenylpropanoid and flavonoid biosynthesis) in cherries treated with melatonin after mechanical damage. In addition, chlorogenate increased slightly during cold storage, with no significant differences between the treatments (Figure 3). It has been observed that when plants are subjected to abiotic stress, genes related to phenylalanine ammonylase (PAL) expression are downregulated; however, expression increases after treatment with exogenous melatonin [24]. In general, melatonin plays an important role in plant growth promotion and anti-stress regulation via efficient radical scavenging and the regulation of antioxidant enzyme activity. In the particular case of cherry, it has been observed that postharvest treatments with exogenous melatonin improve quality attributes such as color, a higher content of phenolic compounds, and anthocyanins along with an increase in the enzymatic antioxidant system have been reported [15,16,18,19]. Moreover, other studies have reported that melatonin treatment improves the contents of total anthocyanins, phenols, and flavonoids in grapes and wine [25] and total phenols and anthocyanins in tomato fruits [26] and delays senescence in kiwifruit leaves through the regulation of antioxidant capacity and flavonoid biosynthesis [27]. It has been reported that the effect of melatonin on flavonoid biosynthesis is due to increased gene expression in these metabolic pathways by reducing promoter methylation, which promotes the synthesis of these compounds [28]. Therefore, in addition to reaffirming that melatonin treatment in cherry increases phenylpropanoid and flavonoid biosynthesis, it can be inferred that the effect of this treatment occurs within a day of application and cold storage, which, to the best of our knowledge, has not been reported before.
Regarding anthocyanin biosynthesis, the metabolite chrysanthemin (cyanidin 3-glucoside) showed higher contents in cherries treated with melatonin during the first 10 d of cold storage (Figure 3). Anthocyanins are the pigments responsible for red, purple, and blue coloration in a wide range of plant tissues and organs and are the main pigments in cherries [29]. They also have multiple functions that are involved in protecting plants from different stresses [30]. Our results show an expected biological sequence in cherries following melatonin treatment, whereby the increase in anthocyanin biosynthesis is related to the phenylpropanoid and flavonoid pathways. It has been widely reported that anthocyanin synthesis can be induced by sugars and hormones, as well as by various environmental factors, such as light and temperature [31,32]. Nevertheless, Chen et al. [29] showed that anthocyanin synthesis in apple trees was higher in fruits exposed to exogenous melatonin, independent of dose, and that pigment accumulation in treated fruit was independent of light exposure. As stated before, this emphasizes the almost immediate effect of melatonin treatment on secondary metabolite biosynthesis during cold storage of sweet cherries.
The stilbenoid, diarylheptanoid, and gingerol pathways involve phenylpropanoid derivatives that provide color, organoleptic, and medicinal properties but also play defensive roles or act as pollinator attractants or seed dispersants in various plant groups [33]. Chlorogenate and p-coumaroyl quinic acid, found in our study, are part of this pathway as well as the aforementioned pathways, which were abundant during cold storage and after melatonin treatment, respectively.
Sphingolipid metabolism and sulfur metabolism (Figure 4 and Table S2) were upregulated after melatonin treatment through the amino acid L-serine (Figure 3). Sphingolipids are structural components of the plasma membrane that function as signaling molecules in response to biotic and abiotic stresses [34]. Moreover, Venable [35] reported that sphingolipids participate in the regulation of cellular senescence and are involved in regulating plant responses to cold stress. However, opposite results have been published regarding sphingolipid metabolism in plants exposed to cold: a decrease in sphingolipids in cold-stored peach fruit [36], but an increase in Arabidopsis [37,38]. This discrepancy may be because harvested fruit does not receive support from the plant, with a decrease in vital metabolism for conservation; in contrast, Arabidopsis was evaluated as a plant receiving vital elements from the environment in which it develops. Sphingolipid biosynthesis in plant cells begins with the production of 3-ketodihydrosphingosine from the amino acid L-serine and by the thioester palmitoyl-CoA catalyzed via serine palmitoyltransferase (SPT) [39]. Our results showed lower contents of L-serine in cherries without melatonin treatment, with a decrease in the regulation of sphingolipid metabolism, similar to that reported by Huang et al. [36] in cold-stored peaches. It is likely that cherry fruits develop symptoms of chilling injury, leading to oxidative damage and lipid peroxidation after mechanical stress [8,13]. The application of postharvest melatonin increased L-serine in sweet cherries, which may promote sphingolipid metabolism. It has been reported that melatonin treatment of cherries delays fruit ripening and senescence, improving resistance to some diseases and cold tolerance [14]. Therefore, it might be possible that the cold tolerance provided by melatonin in cherries is related to the increased metabolism of structural components of the plasma membrane, such as sphingolipids; therefore, melatonin might reduce the incidence of mechanical stress in cherries. However, further studies using higher doses of melatonin must be conducted.
Regarding sulfur, Fatma et al. [40] reported that sulfur metabolism improves photosynthesis in growing plants and reduces the oxidative damage resulting from salt stress. However, there are few studies on sulfur metabolism during fruit postharvest, and although there is evidence that this metabolism influences fruit postharvest quality, the relationship is not entirely clear. An improvement in grape quality was observed after sulfur metabolism was induced by sulfur dioxide treatment [41]. Therefore, the application of melatonin has a beneficial effect on the postharvest quality of cherries, probably through the induction of sulfur metabolism, among other metabolic pathways, that lead to an increase in plant resistance during cold and mechanical stress.
Finally, amino sugar and nucleotide sugar metabolism were significant at the end of cold storage (20 d). The metabolites of this pathway D-fructose and D-xylose showed lower contents after 20 d of cold storage in cherries with melatonin treatment, but the opposite behavior was observed at the beginning of cold storage (Figure 3). These two sugars are predominant in cherry fruits, and changes in their concentrations during ripening and senescence have been reported [42,43]. Although the respiration rate of cherries slow during cold storage, sugars and organic acids are still used to synthesize ATP through glycolysis, the TCA cycle, the pentose phosphate pathway, and oxidative phosphorylation to ensure vital activities [44]. The greater decrease observed in D-xylose and D-fructose in sweet cherries with melatonin treatment during cold storage might be related to an increase in sugar content after melatonin application, providing a greater number of substrates for vital fruit metabolism, which will later be degraded in an expected manner due to prolonged cold storage.
Finally, our results showed that after 20 d of cold storage (with and without melatonin treatment), cherries did not display significant regulation in metabolic pathways related to the biosynthesis of secondary metabolites or of structural compounds of the plasma membrane. Instead, the observed changes were related to the downregulation of amino sugar and nucleotide sugar metabolism in sweet cherries treated with melatonin and prolonged postharvest storage.

5. Conclusions

Our results indicate, when comparing both treatments (400 µM melatonin and control) at day 20 of cold storage, there were no significant differences in the severity of pitting damage. However, when comparing days 10 and 20, it was observed that the melatonin treatment did not have a significant increase in severity as was observed in the control treatment. Since important metabolic changes were observed, it would be interesting to consider a dose–response experiment and evaluate its effect on fruits in cold storage for a longer period of time in future studies. Regarding metabolic pathway expression, our results showed that after a short period of melatonin treatment and cold storage (0 d and 10 d), sweet cherries presented a significant positive regulation in metabolic pathways related to the biosynthesis of secondary metabolites or plasma membrane structural compounds. This finding provides clear evidence that melatonin can modulate the response to mechanical damage. However, it is necessary in the future to deepen the knowledge of the mechanisms triggered by melatonin that seem to induce the metabolism of plasma membrane structural components and those related to mechanical damage.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae9080940/s1, Figure S1: Scale to visually assess surface pitting: 0 = no pitting; 1 = light pitting; 2 = moderate pitting; 3 = severe pitting; and 4 = very severe pitting [45]; Table S1: Targeted and untargeted metabolites of sweet cherry fruit after induced surface pitting treated with melatonin and without melatonin (control) and stored at 1 °C and 95% RH for 0, 10, and 20 d; Table S2: Metabolic pathways and regulation that showed significance at 0, 10, and 20 days of cold storage in sweet cherry with induced mechanical damage.

Author Contributions

Methodology, formal analysis, investigation, writing—review and editing, writing—original draft, I.H.; formal analysis, methodology, E.P. and J.V.; investigation, R.C. and D.C.; conceptualization, writing—review and editing, supervision, R.P.; conceptualization, methodology, writing—review and editing, supervision, C.F. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by Agencia Nacional de Investigación y Desarrollo (ANID) Chile, Fondecyt 1221616, Fondequip EQM140074, and PCI REDBIO0001 grants. R. Pedreschi acknowledges ANID–Millennium Science Initiative Program—ICN2021_044.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

The authors acknowledge the Experimental Station La Palma of Pontificia Universidad Católica de Valparaíso for providing the plant and the fruit materials.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Differences in the severity of pitting damage in sweet cherries with and without melatonin treatment and stored at 1 °C and 95% RH for 0, 10, and 20 d. Different letters indicate statistically significant differences (p value < 0.05) between sweet cherries with melatonin and the control. Fifty fruits were used per replicate (n = 3).
Figure 1. Differences in the severity of pitting damage in sweet cherries with and without melatonin treatment and stored at 1 °C and 95% RH for 0, 10, and 20 d. Different letters indicate statistically significant differences (p value < 0.05) between sweet cherries with melatonin and the control. Fifty fruits were used per replicate (n = 3).
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Figure 2. (A) Score plot of principal component analysis (PCA) of sweet cherries with induced surface pitting treated with melatonin (M) and without melatonin (C) stored at 1 °C and 95% RH for 0, 10, and 20 d. (B) Score plot of partial least squares with discriminant analysis (PLS-DA). Fifty fruits were used per replicate (n = 3).
Figure 2. (A) Score plot of principal component analysis (PCA) of sweet cherries with induced surface pitting treated with melatonin (M) and without melatonin (C) stored at 1 °C and 95% RH for 0, 10, and 20 d. (B) Score plot of partial least squares with discriminant analysis (PLS-DA). Fifty fruits were used per replicate (n = 3).
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Figure 3. Metabolic pathways and metabolites in sweet cherries with induced pitting treated with and without (control) and stored at 1 °C and 95% RH for 0, 10, and 20 d. Asterisk (*) shows significant differences (p value < 0.05). Fifty fruits were used per replicate (n = 3).
Figure 3. Metabolic pathways and metabolites in sweet cherries with induced pitting treated with and without (control) and stored at 1 °C and 95% RH for 0, 10, and 20 d. Asterisk (*) shows significant differences (p value < 0.05). Fifty fruits were used per replicate (n = 3).
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Figure 4. The pathways impact analysis. The metabolic pathways are depicted as circles based on their enrichment scores (y-axis) and topology analyses (pathway impact, x-axis) conducted with MetaboAnalyst 5.0. The intensity of the circle colors (from yellow to red) indicates the extent of significant metabolite changes in each respective pathway.
Figure 4. The pathways impact analysis. The metabolic pathways are depicted as circles based on their enrichment scores (y-axis) and topology analyses (pathway impact, x-axis) conducted with MetaboAnalyst 5.0. The intensity of the circle colors (from yellow to red) indicates the extent of significant metabolite changes in each respective pathway.
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MDPI and ACS Style

Hernández, I.; Ponce, E.; Vidal, J.; Chirinos, R.; Campos, D.; Pedreschi, R.; Fuentealba, C. Metabolomics Reveals Specific Metabolic Changes in Sweet Cherries (Prunus avium L.) Subjected to Postharvest Treatment with Melatonin after Mechanical Stress. Horticulturae 2023, 9, 940. https://doi.org/10.3390/horticulturae9080940

AMA Style

Hernández I, Ponce E, Vidal J, Chirinos R, Campos D, Pedreschi R, Fuentealba C. Metabolomics Reveals Specific Metabolic Changes in Sweet Cherries (Prunus avium L.) Subjected to Postharvest Treatment with Melatonin after Mechanical Stress. Horticulturae. 2023; 9(8):940. https://doi.org/10.3390/horticulturae9080940

Chicago/Turabian Style

Hernández, Ignacia, Excequel Ponce, Juan Vidal, Rosana Chirinos, David Campos, Romina Pedreschi, and Claudia Fuentealba. 2023. "Metabolomics Reveals Specific Metabolic Changes in Sweet Cherries (Prunus avium L.) Subjected to Postharvest Treatment with Melatonin after Mechanical Stress" Horticulturae 9, no. 8: 940. https://doi.org/10.3390/horticulturae9080940

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