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22 June 2022

The Effect of Different Doses of 1-Methylcyclopropene on Postharvest Physiology and Predicting Ethylene Production through Multivariate Adaptive Regression Splines in Cocktail Tomato

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1
Department of Horticulture, Silifke-Tasucu Vocational School, Selcuk University, 33900 Mersin, Turkey
2
Department of Horticulture, Faculty of Agriculture, Van Yuzuncu Yil University, 65080 Van, Turkey
3
Department of Horticulture, Faculty of Agriculture, Ataturk University, 25240 Erzurum, Turkey
*
Authors to whom correspondence should be addressed.
Horticulturae2022, 8(7), 567;https://doi.org/10.3390/horticulturae8070567
This article belongs to the Special Issue Factors Affecting the Quality and Shelf Life of Horticultural Crops
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Abstract

Maintaining the postharvest quality of tomatoes, which are essential in the world vegetable trade, is very important; otherwise, storage may cause severe quality and economic losses. This study aimed to determine the effects of 1-MCP treatments on quality and storage time to prevent quality loss and deterioration in tomatoes due to high temperature and to predict ethylene production through the Multivariate Adaptive Regression Splines algorithm during long-term storage. For this purpose, same-sized fruits were divided into three different groups. Two groups were treated with 1-MCP (625 and 1250 ppb), and the untreated fruit was the control. Then, the tomatoes were stored for 39 days at a temperature of 20 °C and relative humidity of 85–90%. The results obtained from the present study showed that the 1-MCP treatments prolonged the life and maintained the quality of tomato fruit during storage. The ethylene production and respiration rate were significantly lower in 1-MCP-treated fruit than in the untreated fruit during the storage period (p < 0.05). According to the Multivariate Adaptive Regression Splines algorithm, it was observed that increasing doses of 1-MCP inhibited ethylene production. Furthermore, weight loss and respiratory rate were effective on ethylene production at 100 and 43.9%, respectively. In conclusion, treating the fruit with 1250 ppb of 1-MCP was determined to be the best practice for maintaining all quality criteria during storage.

1. Introduction

Tomatoes (Solanum lycopersicum L.) represent the most significant part of the vegetable sector, with 181 million tons of tomatoes grown on an area of approximately 5 million hectares worldwide. Turkey, with a production of 12.8 million tons on approximately 173 thousand hectares, ranks third after China and India, the two most populated countries in the world [1].
The tomato fruit contains rich beneficial phytochemicals and is initially very small. It develops rapidly, matures, and is utilized at various stages, either as whole fresh fruit or used in various products such as conserves, sauces, and juices. Tomatoes synthesize mineral substances, phenolic compounds, antioxidants, vitamins C and E, lycopene, beta carotene, lutein, flavonoids, dehydrotomatine, alpha tomatine, and esculeoside A from glycoalkaloids, which are beneficial for human health by reducing the risk of cancer, heart diseases, and age-related vision disorders [2,3,4].
The color of the skin changes from green to red as the fruit ripens, either on the plant or after harvest, due to the reduction of tomatine, the deterioration of chlorophyll, and the resulting replacement of carotenoids and lycopene. Tomatoes have a short shelf when they are harvested in the red stage due to the high lycopene level. However, in the red stage, the fruit contains high levels of flavor and aroma substances that affect the flavor [5,6]. Because of this, consumers generally prefer red tomatoes. However, red, ripe fruits show more postharvest losses due to their rapid softening, change in acid content, and susceptibility to diseases and disorders. Therefore, fruits are usually harvested during the ripe green or discoloration period to extend the storage and marketing time and minimize postharvest losses [7,8,9,10].
Ethylene is a hormone that promotes the maturation of the fruit, the opening of flowers, and the shedding of leaves. Tomatoes, which continue to mature after harvest, have a climacteric fruit structure. Therefore, tomato is a sample product used in studies investigating the effect of ethylene on the development of climacteric fruit [11]. The uneven discoloration of fruits can be a severe problem in tomato cultivation. In general, tomato fruit is harvested in the mature green, discoloration, pink, light red, and red stages during ripening [12]. Maturation stages and storage temperature affect the nutrient content in tomato fruits [13]. Inhibition of respiration and ethylene production can delay ripening and discoloration. For that purpose, a controlled atmosphere environment with low O2 and high CO2 extends the shelf life of tomatoes by reducing the harmful effects of low temperature and inhibiting ethylene production during storage. Storage at inappropriate temperatures is the leading cause of many postharvest diseases and disorders. Especially in the green period, harvesting and later storage may cause chilling injury. Therefore, storing tomatoes in the red stages could reduce the risk of chilling injury [14,15]. However, it is important to inhibit ethylene production in the storage of red-stage tomatoes; for that purpose, 1-MCP treatments are important to inhibit ethylene production after harvest. 1-MCP is a gas that reduces the effect of ethylene production in plant tissues by linking the ethylene receptor and stopping the ethylene formation signal transmission [16]. Especially in the early period, 1-MCP can be used in tomato storage, together with cultural practices, to prevent early harvest, disperse red color all over, achieve homogeneous maturity, reduce chilling damage, and eliminate bad taste [17].
Different studies have explained the relationships between biochemical and physicochemical parameters (ethylene production and respiratory rate, etc.) using principal component (PCA) and bivariate analyses [18,19,20]. However, more detailed research is needed to reveal the relationships between those variables and explain complex interrelationships. Therefore, alternative statistical techniques are required to reveal linear and non-linear effects between variables. The Multivariate Adaptive Regression Splines (MARS) algorithm is a data mining technique that explains non-linear and interaction effects between predictors and responses. The MARS algorithm reveals the relationship between dependent and independent variables [21].
To our knowledge, there have been few studies on the effects of 1-MCP treatments on tomato fruit stored at high temperatures and no studies using the MARS algorithm for predicting ethylene production. In this study, tomatoes were harvested in the red stage, when the taste and quality values were the highest. The fruit was stored at 20 °C in order to prevent chilling damage, maintain maturity, and retain quality values. The aim of the current study was to determine the effects of 1-MCP treatments on quality and storage time in order to prevent quality loss and deterioration in tomatoes due to high temperature and to predict ethylene production through the MARS algorithm during long-term storage.

2. Materials and Methods

The tomato fruits (Solanum lycopersicum L. cv ‘Seyit F1’ cocktail tomato) used in the study were obtained from a geothermally heated hydroponic greenhouse from a commercial company located in the Van province in Turkey (39°07′26 N, 43°52′06 E). The fruit was harvested at the red stage and pre-cooled for 24 h in cold storage at a temperature of 10 °C and relative humidity of 85–90%. 1-MCP treatments were applied to tomato fruit at a rate of 625 and 1250 ppb at 20 °C for 24 h, and 210 ± 10 g of the fruit were placed in transparent glass jars with a lid with a volume of 600 mL, which contained a gas permeable medium. Then, the tomato fruits were stored for 39 days at a temperature of 20 °C and relative humidity of 85–90%. Physical and biochemical analyses were performed on days 0, 7, 12, 17, 28, and 39 to control the quality values during storage.

2.1. Weight Loss

Weight loss over the storage period was measured daily and calculated as a percentage of the initial weight.

2.2. Soluble Solids Content (SSC), Fruit Juice pH, Titratable Acidity (TA)

Titratable acidity (TA) was analyzed by adding 0.1 N NaOH of fruit juice until pH = 8.1, and the results were expressed as percentage citric acid [22]. pH values were measured with a pH meter in fruit juice (Mettler-Toledo, Columbus, OH, USA). Soluble solids content (SSC) was measured by a digital handheld refractometer (Atago, Tokyo, Japan), and the results are expressed as percentages.

2.3. Color

Fruit skin color was measured by a chromameter (Minolta CR-400; Osaka, Japan) in L, a and ΔE.

2.4. Total Phenolic Content (TPC) and Antioxidant Capacity (AC)

Total phenolic content was determined with a spectrophotometer (Genesys 10S UV-VIS, Thermo Scientific, Waltham, MA, USA) at 725 nm and was assessed in gallic acid equivalent (GAE) mg100 g−1 FW. The Ferric Reducing Antioxidant Power (FRAP) method was utilized to evaluate the total antioxidant capacity at 593 nm and was assessed in μmol Trolox equivalent (TE) g−1 FW [22].

2.5. Antioxidative Enzyme Analyses

The activity of superoxide dismutase (SOD), catalase (CAT), and Ascorbate peroxidase (APX) enzymes was spectrophotometrically measured at 560, 240, and 290 nm, respectively [23]. The levels of lipid peroxidation were assessed as malondialdehyde (MDA) content [23].

2.6. Respiration Rate and Ethylene Production

The fruit was placed in closed jars for 2 h, and the CO2 emission of fruit was detected in the headspace gas sample with the Headspace Gas Analyzer GS3/L analyzer. The respiration rate values are expressed as mL CO2 kg−1 h−1 [24]. The ethylene production of the fruit kept in jars for 2 h was analyzed through a gas-tight syringe and injected with a GC-FID (GC-2010 Plus). The ethylene production was expressed as μL C2H4 kg−1 h−1 [24].

2.7. Statistical Analysis

This study was conducted in a completely randomized design with three replications, and each pack was considered one replicate. Descriptive statistics for the variables studied were shown as Mean and Standard Error of Mean (SEM). Two-way Factorial ANOVA was applied to the data. The 1-MCP concentrations and storage period were evaluated factors. Duncans’ Multiple Range Test comparisons were also used to identify different treatment and storage factors. The statistical significance level was accepted as 5%, and the SPSS (ver. 20) statistical program was used for all statistical calculations.
Ethylene production model: The MARS analysis was performed using the earth package of R software (ver. 4.1.3) [25]. The algorithm was applied to determine the effect of dependent and independent variables on the prediction of ethylene production. The 1-MCP concentrations and storage period were evaluated factors. The MARS model building process consists of forward and backward stepwise selections to define the knots and splines. First, the model is overfitted by forward selection of more basis functions than required to express the response variable, and subsequently, backward pruning is performed by deleting the least significant splines one at a time until an optimal model is obtained. The model is refitted after each basis function removal, and each reduced sub-optimal model is tested with the Generalized Cross-Validation (GCV) method to prevent overfitting. The goodness of fit criteria was provided with root-mean-square-error (RMSE) and standard deviation ratio (SD) for predicting the performance of MARS.

3. Results

3.1. Weight Loss

In the study, the highest weight loss was observed in the control fruit (7.83%), while the lowest was found in the treatment of 1250 ppb 1-MCP (2.74%) at the end of the storage period. Although the tomato fruit was stored at a high relative humidity of 90%, water loss could increase due to high temperature-induced respiration rate and transpiration. In addition, the harvesting of fruits in the red stage period was another factor that caused a decrease in the water content of the fruit due to the increase in the amount of soluble solids content. Weight loss was significantly (p < 0.05) lower in 1-MCP-treated fruit than in the control fruit (Table 1).
Table 1. The weight loss during storage of ‘Seyit F1’ cocktail tomato (Solanum lycopersicum L.). Data are presented as means ± SEM.

3.2. Soluble Solids Content (SSC), Fruit Juice pH, Titratable Acidity (TA)

The pH level and soluble solids content (SSC) were determined at the highest level in the control fruit and lower levels in the fruit treated with 1-MCP treatments (Table 2). Titratable acidity (TA) was determined at the highest level in the fruit treated with 1-MCP treatments (Table 2).
Table 2. The SSC, pH, and TA during storage of ‘Seyit F1’ cocktail tomato (Solanum lycopersicum L.). Data are presented as means ± SEM.

3.3. Color (L, a, and ΔE)

In the current study, it was observed that there was a regular decrease in L value from the beginning to the end of storage, whereas there was a regular increase in a and ΔE values, depending on the ripening during the storage period (Table 3). L* value was significantly higher in 1-MCP-treated fruit, but a* and ΔE values were lower than in the control fruit (p < 0.05).
Table 3. The L*, a*, and ΔE during storage of ‘Seyit F1’ cocktail tomato (Solanum lycopersicum L.). Data are presented as means ± SEM.

3.4. Antioxidative Enzymes (APX, CAT, and SOD) and Lipid Peroxidation (MDA)

There was an increase in APX, CAT, and SOD enzyme activities on the 12th day of storage, and then a decrease was found in all treatments during the storage period. The highest APX, CAT, and SOD enzyme activities were observed in fruit treated with 1250 ppb 1-MCP treatment during storage (Table 4 and Figure 1). On the other hand, there was a regular increase in the MDA level during storage; the highest rate was determined in the control fruit as well (Table 4 and Figure 1). The activity of APX, CAT, and SOD enzymes was significantly higher in 1-MCP-treated fruit, while the level of MDA was lower in 1-MCP-treated fruit than in control fruit during storage (p < 0.05).
Table 4. The APX, CAT, SOD, and MDA during storage of ‘Seyit F1’ cocktail tomato (Solanum lycopersicum L.). Data are presented as means ± SEM.
Figure 1. The APX, SOD, CAT, and MDA during storage of ‘Seyit F1’ cocktail tomato (Solanum lycopersicum L.).

3.5. Total Phenolic Content and Antioxidant Capacity

Fluctuations in both total phenolic content and antioxidant capacity during the storage were observed. However, total phenolic content and antioxidant capacity were significantly higher in 1-MCP-treated fruit than in the control fruit during the storage period (p < 0.05). Moreover, 1250 ppb 1-MCP-treated fruit had the highest antioxidant capacity and total phenolic content (Table 5).
Table 5. The total phenolic content and antioxidant capacity during storage of ‘Seyit F1’ cocktail tomato (Solanum lycopersicum L.). Data are presented as means ± SEM.

3.6. Ethylene Production, Respiration Rate, and Ethylene Production Model

As described in Figure 2, ethylene production and respiration rate were significantly lower in 1-MCP-treated fruit than in untreated fruit during the storage period (p < 0.05).
Figure 2. The ethylene production and respiration rate during storage of ‘Seyit F1’ cocktail tomato (Solanum lycopersicum L.) The differences among treatments are shown with capital letters for the same storage period (p < 0.05).
The MARS model for predicting multiplication (Table 6), if it is weight loss > 1.57, pH < 4.35, respiration rate < 21.3, antioxidant capacity > 7.97, and a < 22.6, ethylene production could be lower. In addition, according to the MARS algorithm, the control group fruit, which was not treated at all, had an effect of 1.96 μL C2H4 kg−1 h−1 on ethylene production. This situation indicates that 1-MCP application actually inhibits ethylene production compared to control fruit.
Table 6. Basic functions and corresponding coefficients of the Multivariate Adaptive Regression Splines (MARS) model for ethylene production prediction in tomato fruit during storage period.
As the storage time continues, low ethylene production occurs with increases in weight loss due to senescence. However, in general, lower ethylene production is desired with the maintenance of lower weight loss during storage. Therefore, considering the lower weight loss, the best values for the prediction of ethylene production were ensured by 1250, 625 ppb 1-MCP, and the control group, respectively. If the standard deviation ratio is less than 0.10, it indicates that the model is a very good fit for prediction [19]. We found that the SD ratio and RMSE were 0.045 and 0.098, respectively, in the present study.

4. Discussion

Tomatoes are climacteric fruit; respiration and vitality events continue after harvest, and an increase in maturity results in significant changes in color, aroma, taste, and fruit texture. If it is thought that harvesting green and pink stage tomatoes, which are intended to be stored for a long time, will increase the storage and marketing time, this would be the wrong approach. Because tomato fruits with red color stay on the plant longer and contain more photosynthesis products, the taste and aroma are better, and the risk of chilling is eliminated. Some previous research [15] demonstrated in their studies that weight loss and physiological deterioration, especially chilling damage, is more common in fruit harvested in the early stage during cold storage.
We found that 1-MCP application slowed down ethylene production in climacteric fruits such as tomatoes, leading to a reduced weight loss related to low ethylene production and respiration rate [26]. Similarly, it was suggested that weight losses decreased in previous studies that used 1-MCP to store tomato fruits [27,28,29,30]. Similar results were obtained from the current study, where the 1-MCP-treated fruit showed lower weight loss than the control fruit.
The decrease in the amount of SSC as a result of excessive ripeness in tomato fruit occurs due to the degradation of polysaccharides during ripening [31,32]. As a result of this situation, SSC values continue to increase until the highest standard value of the variety and then decrease due to the effect of environmental and nutritional conditions, resulting in the fruit softening and deteriorating. In the current study, since the storage of fruit was terminated at 39 days without showing any softening and deterioration, the SSC values, especially the control fruit, increased continuously. In the case of prolonged storage, it is expected that the SSC values of tomatoes could decrease with deterioration, and softening due to the use of organic acids in the respiration process. The results obtained from the present study are similar to previous studies [32,33,34,35].
The amount of TA in tomato fruit, which is high in the green and pink stages, decreases as an indicator of maturity due to the ripening, the formation of dark red color, and use in the respiration process [36]. In previous studies, the TA decreased in the red mature period, similar to the current study [6,33,35]. Furthermore, it was noted that TA was retained more in fruit treated with 1-MCP than in untreated tomato fruit [37]. In the present study, we supported the aforementioned studies where TA was higher in fruit treated with 1-MCP than in control fruit during storage. In previous research, it was determined that the pH value of tomatoes harvested during the red stage period and stored in controlled atmospheres (CA) containing high carbon dioxide content remained at a low level, similar to the current study [38].
Chlorophylls, which give a green color, are deteriorated as the color turns to red, and the amount of lycopene, which creates the red color, increases related to ripening and the ambient temperature in tomatoes [39]. However, it is known that 1-MCP treatments slow down chlorophyll deterioration. It was reported in different studies that 1-MCP treatments maintained brightness and retained color changes in tomato fruit harvested in the red stage during storage [6,38,40,41].
In tomatoes, deterioration increases after redness, especially in a high temperature and oxygen environment. Antioxidative enzymes such as APX, CAT, and SOD are involved in senescence, and the defense system plays a vital role in suppressing oxidative stress. The defense system protects cells from oxidative damage by preventing the accumulation of free oxygen radicals [23,42]. In previous studies, similar to the current study, it was determined that CAT, SOD, and APX enzyme activity was higher in 1-MCP-treated fruit, while MDA content was lower than in control fruit [43,44,45]. In general, during the ripening of red tomatoes, chlorophyll molecules are degraded by enzymes, and the green color disappears on the fruit skin [6]. However, in the present study, it can be stated that deterioration, softening, and loss of color changes were retained by increasing the activity of CAT, SOD, and APX enzymes with the 1-MCP treatment in tomatoes. Thus, senescence was delayed during the storage period.
In particular, the content of total phenolic and antioxidant capacity may vary depending on the variety, environmental factors, growing techniques, and storage conditions [46]. It was reported in previous studies that the highest total phenolic and antioxidant activity was found in tomato fruit harvested at color breakage and full redness [32,47]. In the current study, total phenolic content and antioxidant capacity reached the highest level on the seventh day of storage and then decreased. In the light of the aforementioned information, it can be said that this situation is due to the fact that the seventh day of storage is the beginning of maturity and storage at 20 °C. We obtained similar findings in earlier studies where 1-MCP treatment enhanced total phenolic content and antioxidant capacity [46,48,49,50,51].
1-MCP blocks ethylene production in plant tissues by linking to ethylene receptors [16]. In the present study, ethylene production decreased in tomato fruit during storage compared to control fruit. A similar pattern was observed in that respiration rate decreased continuously except for control and 625 ppb 1-MCP treatments on the seventh day of storage. In addition, ethylene decreased rapidly in the first seven days of storage, but then this decrease slowed down. Furthermore, in previous research [52], it was determined that tomatoes treated with 1-MCP had a lower respiration rate and reduced ripening compared to the control fruit, similar to the present study.

5. Conclusions

In this study, tomatoes harvested in the red stage at full maturity were stored at high-temperature values of 20 °C in order to have high quality and flavor values and to reduce chilling damage. 1-MCP was applied to slow down ripening and extend storage and shelf life. In general, there is a negative relationship between the delay of maturity in tomatoes with 1-MCP and the storage temperature, and there have been not many studies on high-temperature storage of tomatoes [53]. In this respect, the study is important as it sheds light on future studies.
Pearson’s Correlation explains the relationships between the variables, but these relationships are insufficient to reveal as percentages. On the other hand, the MARS algorithm enables the expression of one or more desired features with other variables as a percentage. In the current study, weight loss, respiratory rate, antioxidant capacity, pH, and a* value were found to be effective on ethylene production at 100, 43.9, 35.4, 19.4, and 4.9%, respectively (Table 7).
Table 7. The effect of variables on ethylene production prediction, using the Multivariate Adaptive Regression Splines (MARS) model in tomato fruit. Data are shown as percentages.
As a result, fruit treated with 1250 ppb 1-MCP was found to be the best practice in maintaining all quality criteria during storage. It has been determined that 1-MCP treatments in tomatoes are commercially recommendable in terms of ease of treatment and environment-friendly treatment, leaving no residue, and no information about its negative impact on human health has been detected so far.

Author Contributions

Conceptualization, A.B., S.C., N.Y., O.T. and S.E.; methodology, A.B. and S.C.; formal analysis, A.B., S.C., N.Y. and O.T.; data curation, A.B. and S.C.; writing—original draft preparation, A.B., S.C., N.Y., O.T. and S.E.; writing—review and editing, A.B. and S.C.; supervision, A.B., S.C. and S.E. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Researchers Supporting Project number (FBA-2021-9232), Department of Scientific Research Projects (BAP), Van Yuzuncu Yil University, Turkey.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All related data are within the manuscript.

Acknowledgments

The authors would like to extend their sincere appreciation to the Researcher Supporting Project number (FBA-2021-9232), Department of Scientific Research Projects (BAP), Van Yuzuncu Yil University, Turkey.

Conflicts of Interest

The authors declare no conflict of interest.

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