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Article

Time–Course Analysis of the Onset and Progression of Cuticle Cracking in Fruits of Cherry Tomato Cultivar ‘Nene’

by
Ryosuke Hosoi
1,
Kazuo Ikeda
1,2,
Takashi Nishizawa
2 and
Tomoyuki Nabeshima
1,2,*
1
United Graduate School of Agricultural Sciences, Iwate University, Tsuruoka 997-8555, Japan
2
Faculty of Agriculture, Yamagata University, Tsuruoka 997-8555, Japan
*
Author to whom correspondence should be addressed.
Horticulturae 2025, 11(1), 89; https://doi.org/10.3390/horticulturae11010089
Submission received: 16 December 2024 / Revised: 10 January 2025 / Accepted: 12 January 2025 / Published: 15 January 2025
(This article belongs to the Section Biotic and Abiotic Stress)
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Abstract

:
Cuticle cracking in tomatoes, characterized by fine cracks on the cuticular membrane, significantly reduces their shelf life. In this study, we collected basic information about the onset and progression of cuticular cracks in cherry tomatoes by observing the time–course of cuticular cracks incidence and severity during three cultivation periods. Several fruit characteristics—including the fruit weight, cuticular membrane deposition, and epidermal cell morphology—were analyzed alongside environmental factors to identify the conditions under which cuticular crack occurs. In the spring–summer season, cuticular cracks’ onset occurred at 30 days after anthesis, whereas in the summer–autumn, it occurred at 20 days after anthesis. The severity of cuticular cracks at harvest was higher in the summer–autumn cultivation than in the spring–summer. These results indicate that the period during which susceptibility to cuticular cracks increases may vary by season, contributing to seasonal differences in the final severity. However, no consistent relationship was observed between the incidence or severity of cuticular cracks and the fruit size, temperature, or humidity throughout the study. In both seasons, the onset of cuticular cracks coincided with the peaking of the cuticular membrane deposition. Thickening of the cuticular membrane, resulting in decreased elasticity may contribute to the cuticular cracks’ onset.

1. Introduction

The outer surface layer of the epidermal cell wall in land plants is covered by a cuticular membrane (CM), which is composed of cutins, epi-cuticular waxes, intra-cuticular waxes, polysaccharides, and phenolics [1,2,3,4,5,6]. The CM acts as a barrier to reduce water loss from the tissue while protecting against pathogen and insect infection [7,8,9,10,11,12]. Maintaining its integrity is crucial for preserving fruit quality during development and postharvest [13]. However, skin disorders frequently arise due to cracking of the CM, significantly reducing the shelf life of fruit [14]. In tomato (Solanum lycopersicum), cuticular crack manifests as very fine hair-like cracks on the CM, oriented in all directions on the sides and bottom of fruit, rendering a net-like appearance to the surface of the fruit [15,16]. The occurrence of cuticular cracks on fruits results in economic losses, as it reduces the shelf life and increases the pathogen susceptibility of fruits [17]. In the relative absence of stomata from tomato fruit [18], predominant water loss is through the cuticle, making any cuticular cracks more relevant than on other fruit with stomata. The occurrence of cuticular cracks was first reported by Young [19]. These cracks have been described using various terms, such as hair cracking, swell cracking, shrink cracking, rain check, or cuticle blotch [15,20,21]. Since cuticular cracks are microscopic, identifying their occurrence with the naked eye is difficult and requires considerable experience. The substantial labor incurred in sorting fruits with cuticular cracks reduces the pack-out of tomato fruit. Thus, development of tolerant genotypes or practical methods for managing cuticular cracks is desirable.
The occurrence of cuticular cracks is affected by cultural and environmental factors, as well as by anatomical aspects [15,21]. The cultural factors include the leaf-to-fruit ratio [22] and boron deficiency [23]; environmental factors include fluctuations in the temperature [15,24], relative humidity (RH) [15,24], and radiation [15]; and anatomical aspects include the CM thickness [21,25], CM mechanical properties [26], and fruit size [21,22]. Moreover, the timing of cuticular cracks onset varies among cultivars. In the medium-sized tomato cultivar ‘Calypso’, the onset of cuticular cracks was observed approximately 40 days after fruit set [27]. The onset of cuticular cracks in ‘Fla. 7181’ was observed in only 2% fruits at the immature green stage, while 61% of fruits exhibited cuticular cracks at the mature green (MG) stage [28]. In the beefsteak (large-sized) tomato ‘Rapsodie’, cuticular cracks occurred 2 weeks after the maximum relative growth rate of the fruit was achieved [16]. These findings indicate that the onset of cuticular cracks is a complex physiological disorder influenced by the cultivar, fruit development stage, and environmental factors. Methods, such as the foliar application of boron or calcium [29,30] and greenhouse shading [15], have been reported to reduce cuticular cracks’ incidence. To effectively apply these control measures or develop new techniques, it is essential to elucidate the relationships among the cultivar, environmental conditions, and the timing of cuticular cracks’ onset. In recent years, the demand for cherry tomatoes has surged in countries such as Japan, the United States, Canada, Thailand, and Germany [31]. However, previous studies on cuticular cracks have primarily focused on medium- and large-sized tomatoes, and information pertaining to cherry tomatoes is relatively scarce.
In this study, we aimed to collect basic information on the onset and subsequent progression of cuticular cracks in cherry tomatoes. Previously, we observed that severe cuticular cracks are more likely to occur in fruits that develop without fertilization and in those with a smaller size [32]. However, fruit set via parthenocarpy did not correlate with the onset or frequency of cuticle cracking. To eliminate the effects of natural parthenocarpy and the resulting insufficient fruit enlargement, we selected ‘Nene’ as a model cultivar for cuticle cracking research in cherry tomatoes due to its facultatively parthenocarpic trait. This trait ensures that fruit set and enlargement are unaffected by pollination and fertilization at anthesis, thereby preventing contamination from cuticular cracks associated with limited fruit enlargement. We also investigated the fruit weight, epidermal cell density, and CM accumulation to determine the fruit characteristics and environmental factors related to the occurrence of cuticular cracks in cherry tomatoes.

2. Materials and Methods

2.1. Plant Materials and Cultivation

Tomato plants were grown from seeds from 25 July to 11 November in 2022 (hereafter, called 2022 summer–autumn cultivation), from 15 March to 30 June in 2023 (2023 spring–summer cultivation), and from 25 July to 28 October in 2023 (2023 summer–autumn cultivation). Seeds of ‘Nene’ were sown in 36-well plastic trays filled with commercial mixed soil (N:P:K = 220:550:210 mg·L−1, Pot Baido 300, Tsuruoka City Agricultural Cooperative, Tsuruoka, Japan) on 25 July for the 2022 summer–autumn cultivation, on 15 March for the 2023 spring–summer cultivation, and on 25 July for the 2023 summer–autumn cultivation. Subsequently, the trays were placed in a growth chamber at 25 °C under a 16:8 h light:darkness photoperiod to facilitate germination. The seedlings, thus obtained, were transplanted into 120 mm plastic pots and placed in a greenhouse located in the experimental field of Yamagata University, Tsuruoka, Japan (38°44′ N, 139°49′ E) on 12 August for the 2022 summer–autumn cultivation, on 31 March for the 2023 spring–summer cultivation, and on 8 August for the 2023 summer–autumn cultivation. All the plants were transplanted into 10 L pots containing commercial mixed soil on 26 August for the 2022 summer–autumn cultivation, on 20 April for the 2023 spring–summer cultivation, and on 26 August for the 2023 summer–autumn cultivation. Side shoots were pruned from all plants to achieve a single stem. The plants were allowed to grow until they developed three trusses. The main stem was pruned, leaving one leaf above truss 3. All trusses were pinched to make 12 fruits/truss when the twelfth flower bloomed. Fruits used for subsequent analyses were obtained from the 5th to 8th positions, counting from the base of trusses 1 and 2. We recorded the date of anthesis of these flowers and harvested the fruits at 10, 20, 30, and 40 days after anthesis (DAA). We used 63, 40, and 40 plants in the 2022 summer–autumn, 2023 spring–summer, and 2023 summer–autumn cultivation, respectively. Sixty-seven to 118 fruits were harvested for each DAA. Fertilizers (N:P:K = 60:80:60 mg·g−1, Rakuyo, Kyoto, Japan) were applied at a rate of 20 g·pot−1 on September 13 for the 2022 summer–autumn cultivation, on May 11 for the 2023 spring–summer cultivation, and on 17 September for the 2023 summer–autumn cultivation. The daily air temperatures and RH were recorded once every 15 min using a thermos recorder (RTR-503, T&D corporation, Nagano, Japan).

2.2. Determination of Fruit Size and Onset of Cuticular Cracks

The fruit weight was measured using an electronic balance (ATX224; Shimadzu Co., Kyoto, Japan). The equatorial diameter and height of fruits were measured using a digital caliper (19978, Shinwa Rules Co., Ltd., Niigata, Japan). The average of the measured diameters was used to calculate the surface area of the fruit, considering that the fruit was spherical. To assess the severity of cuticular cracks, the surface of each fruit was observed at four points equally spaced along the equator. The observed fruit surface was categorized into five groups based on the severity of cuticular cracks as follows: grade 0 (fruits without cuticular cracks), grade 1 (fruits with cuticular cracks, approximately <300 µm in length, with most cuticular cracks not connected to each other), grade 2 (fruits with cuticular cracks, having a maximum length of approximately >300 µm, with half of cuticular cracks not connected to each other), grade 3 (fruits with cuticular cracks connected to each other, with approximately half of the field of view covered with connected cuticular cracks), and grade 4 (fruits with cuticular cracks, forming a net-like structure, with almost the entire fruit surface under view covered with cuticular cracks) (Figure 1).

2.3. Measurement of CM Deposition and Epidermal Cell Density

The harvested fruits were bisected, with the sections passing through the pedicel and blossom end. They were then incubated in a 50 mM acetic acid buffer (pH 4.0) containing pectinase (3 g·L−1) (Pectinase SS, Yakult pharmaceutical industry Co., Ltd., Tokyo, Japan) and cellulase (4 g·L−1) (Cellulase Y-NC, Yakult pharmaceutical industry Co., Ltd.) at 55 °C for at least 2 weeks. The enzyme solution was refreshed once a week during the incubation period. After the incubation, the isolated CMs were dried completely at 40 °C and then weighed to calculate the amount of CM deposition per fruit surface area. We did not use fruits harvested at 10 DAA in the 2023 spring–summer cultivation for this analysis because of the difficulty in isolating CM from immature small fruits. In a few samples, CMs with lignified scars were observed and were excluded from analysis.
In tomatoes, the CM on the fruit epidermis forms wedge-shaped protrusions that extend into the anticlinal walls of epidermal cells. These protrusions retain their shape even after the isolation of CM, making them valuable for the morphological analysis of epidermal cells. Images were taken at four equally spaced points along the equator of the fruit using an optical microscope (DM2500 LED, Leica, Tokyo, Japan) equipped with a camera (MC 190 HD; Leica, Tokyo, Japan). The density of the epidermal cells was observed on all four sides. To estimate the epidermal cell density, each cell that fell entirely within the image (275.53 µm × 206.65 µm) was counted as one cell, whereas a cell that crossed the frame boundary of the image was counted as 0.5 of a cell.

2.4. Statistical Analyses

Statistical analyses were conducted using EZR ver. 1.41 [33]. Tukey’s honestly significant difference (HSD) test was performed to compare the means of the fruit weight and CM deposition across cultivation seasons. Additionally, Tukey’s HSD test was used to compare the means of the fruit weight, CM deposition, fruit height, fruit diameter, and length-to-width ratio among cuticular crack severity on the specified DAA. If only one sample was available for a given severity, it was excluded from statistical analysis. The t-test was performed to compare the means of the epidermal cell density, temperature, and RH between the fruit with cuticular cracks and without cuticular cracks. All statistical analyses were performed at a 5% significance level.

3. Results

3.1. 2023 Spring–Summer Cultivation

The daily mean temperature during the 2023 spring–summer cultivation period was 19.0 °C in May when anthesis in the first and second trusses was observed, 24.2 °C in June, and 26.9 °C in July, demonstrating a gradual increase throughout the growing season (Figure 2A). No drastic change in the daily mean RH was observed during the same period (66.7% in May, 69.5% in June, and 72.1% in July) (Supplementary Figure S1A). However, large daily variations, attributed to weather conditions, were observed over the growing season (Supplementary Figure S1A). During this cultivation period, ‘Nene’ fruits exhibited rapid growth between 10 and 20 DAA, with a growth rate of 0.92 g·day−1, which was slightly reduced to 0.74 g·day−1 from 20 to 30 DAA (Figure 3A). The fruit weight reached approximately 20 g at 30 DAA, with negligible further growth observed between 30 and 40 DAA (Figure 3A). The fruit development reached the MG stage around 30 DAA and progressed to the red-ripe stage by 40 DAA. CM deposition was markedly increased from 1.6 to 2.7 mg·cm−2 between 20 and 30 DAA, reaching its maximum at 30 DAA (Figure 3B). At 40 DAA, the CM deposition remained consistent with that at 30 DAA, being 2.6 mg·cm−2 (Figure 3B). At 10 DAA, CM deposition could not be determined because of the difficulty in handling very thin CM at this time point.
Almost all fruits in the 2023 spring–summer cultivation exhibited grade 0 at 10 and 20 DAA, but the onset of cuticular cracks was first observed at 30 DAA, with incidences of cuticular cracks in grade 1, grade 2, grade 3, and grade 4 at 33%, 1%, 0%, and 0%, respectively (Figure 4). These values increased to 49%, 10%, 1%, and 3% at 40 DAA, indicating that the severity of cuticular cracks increased between 30 and 40 DAA (Figure 4). In total, 37% of fruits remained without cuticular cracks at 40 DAA (Figure 4). In fruits harvested at 30 DAA, the grade 1 fruits exhibited a significantly higher fruit weight and CM deposition compared to the grade 0 fruits (Table 1). At 30 DAA, the grade 1 fruits exhibited a significantly greater fruit height and fruit diameter, although no significant differences were observed in the length-to-width ratio among the different cuticular crack severities (Supplementary Table S1). This suggests that the higher fruit weight in grade 1 fruits was not due to an unbalanced enlargement but rather due to an overall enlargement of the fruit. These variations in fruit size and CM deposition between different cuticular cracks severities were not observed at 40 DAA (Table 1). Since, in a previous study [23,32], we identified a negative correlation between the epidermal cell density and cuticular crack severity in cherry tomatoes, we additionally explored the relationship between the cuticular cracks’ onset and the epidermal cell density (Table 2). However, no significant differences were found in the epidermal cell density between the fruit with cuticular cracks and without cuticular cracks at 30 and 40 DAA (Table 2).

3.2. 2022 and 2023 Summer–Autumn Cultivations

A comparison of the environmental conditions during the summer–autumn cultivation periods of 2022 and 2023 revealed a gradual decrease in temperature throughout the growing seasons (Figure 2B). In 2022, the daily mean temperature was 25.0 °C in September, when anthesis of the first and second trusses was observed, and it decreased to 17.9 °C in October. In contrast, the daily mean temperature in 2023 was slightly higher at 27.1 °C in September, and it dropped to 17.3 °C in October. The RH values were 73.2% in September and 77.7% in October 2022, whereas in 2023, they were 71.5% and 72.1%, respectively (Supplementary Figure S1B). In both years, daily variations in RH due to changing weather conditions were observed (Supplementary Figure S1B). In the 2022 summer–autumn cultivation, ‘Nene’ fruits exhibited rapid growth, with growth rates of 0.77 and 0.57 g·day−1 from 10 to 20 DAA and from 20 to 30 DAA, respectively, and the final fruit weight was approximately 20 g (Figure 3A). In the 2023 summer–autumn cultivation, the fruit growth rate from 10 to 20 DAA (0.78 g·day−1) was almost identical to that in the 2022 summer–autumn cultivation, whereas it was lower (0.20 g·day−1) from 20 to 30 DAA and increased slightly (0.30 g·day−1) from 30 to 40 DAA, resulting in a final fruit weight of approximately 16 g (Figure 3A). The fruit development reached the breaker stage around 30 DAA and the red-ripe stage by 40 DAA. At 30 DAA, the maturity stage of fruits was more advanced in both the summer–autumn cultivations compared to the 2023 spring–summer cultivation. However, no differences in fruit maturity stages were observed between the 2022 and 2023 summer–autumn cultivations. In both the 2022 and 2023 summer–autumn cultivations, the CM deposition was markedly increased from approximately 1.0 mg·cm−2 to approximately 2.0 mg·cm−2 between 10 and 20 DAA, reaching near its maximum level at 20 DAA (Figure 3B). At 40 DAA, the CM deposition remained consistent with that at 20 DAA, being 2.4 mg·cm−2 in the 2022 summer–autumn cultivation and 2.3 mg·cm−2 in the 2023 summer–autumn cultivation (Figure 3B).
In both the 2022 and 2023 summer–autumn cultivations, almost all fruits showed grade 0 at 10 DAA, and cuticular crack onset was observed in approximately half of the fruits at 20 DAA (Figure 4). In the summer–autumn cultivations of 2022 and 2023, almost all fruits exhibited cuticular cracks at 30 DAA. Similar to the 2023 spring–summer cultivation, the incidence and severity of cuticular cracks increased from 30 DAA (the onset stage) to 40 DAA (Figure 4). At 20 DAA, grade 1, grade 2, grade 3, and grade 4 occurred in 45%, 5%, 0%, and 0% of the fruits, respectively, in 2022, and in 45%, 3%, 0%, and 0% of the fruits, respectively, in 2023 (Figure 4). Thus, the distribution of cuticular crack severity at 20 DAA was nearly identical in 2022 and 2023. However, the progression of the severity was more pronounced in 2022, with the proportion of the most severe grade 4 cases at 40 DAA reaching 32% in 2022 compared with 17% in 2023. In fruits harvested at 20 and 30 DAA in both the 2022 and 2023 summer–autumn cultivations, no significant differences in the fruit weight, fruit diameter, height, and length-to-width ratio were observed among the cuticular crack severities (Table 1 and Supplementary Table S1). Significant differences in the fruit weight, fruit diameter, and height and length-to-width ratio among cuticular crack severities were observed only at 40 DAA in the 2022 summer–autumn cultivation, with grade 4 fruit exhibiting the lowest fruit weight and smallest fruit diameter (Table 1 and Supplementary Table S1). At 20 DAA, no significant difference in CM deposition was observed among the four categories based on cuticular crack severity (Table 1). However, the CM deposition was greater in grade 4 fruit at 40 DAA in the 2022 summer–autumn cultivation and at 30 DAA in the 2023 summer–autumn cultivation. At 20 DAA, no significant differences in the epidermal cell density were observed between fruits with cuticular cracks and without cuticular cracks in both the 2022 and 2023 summer–autumn cultivations (Table 2).
In summary, we observed an earlier onset of cuticular cracks and higher frequency of severe cuticular cracks in the middle-to-last phase of fruit growth in the summer–autumn cultivations compared with that in the spring–summer cultivation. The severity of cuticular cracks also differed between the 2022 and 2023 summer–autumn cultivations probably due to the difference in environmental factors or fruit growth characteristics between the two cultivations. Similar to the results for the spring–summer cultivation, no consistent trend was observed in the relationship between cuticular crack severity and fruit weight, shape, and CM deposition.

3.3. Analysis of the Relationship Between Cuticular Cracks’ Onset and Environmental Factors

In view of the seasonal differences in the timing of cuticular cracks’ onset, we further investigated the relationship between cuticular cracks’ onset and environmental factors. Figure 5 and Supplementary Figure S2 illustrate the relationship between the anthesis date and cuticular crack incidence for fruits harvested at 20 DAA (in both the summer–autumn cultivations) or 30 DAA (in the 2023 spring–summer cultivation) across the cultivation seasons. In the 2022 summer–autumn cultivation, the cuticular cracks’ incidence decreased toward the latter part of the growing season, reaching 0% after 14 September. However, in the 2023 spring–summer and 2023 summer–autumn cultivations, the cuticular cracks’ incidence remained stable throughout the growing seasons without any notable fluctuation. We analyzed the effects of the temperature and RH on the cuticular cracks’ onset, focusing on the environmental conditions experienced by fruits from the date of anthesis to the assumed onset of cuticular cracks (20 days for both the summer–autumn cultivations and 30 days for the 2023 spring–summer cultivation). As an example, Figure 6 illustrates the relationship between the onset of cuticular cracks and the accumulated temperature. In the 2022 summer–autumn cultivation, fruits that exhibited cuticular cracks were exposed to higher accumulated temperatures than fruits without cuticular cracks (Figure 6). However, no clear relationship was observed for the 2023 spring–summer and 2023 summer–autumn cultivations (Figure 6). Similarly, further analyses of the relationships between cuticular cracks’ onset and other environmental parameters—including maximum, minimum, daily, daytime, and nighttime temperatures (Supplementary Figures S3–S7), day/night temperature differences (Supplementary Figure S8), and RH (Supplementary Figure S9)—revealed no consistent trends for the analyzed parameters.

4. Discussion

4.1. Onset of Cuticular Cracks

The occurrence of cuticular cracks has been reported under various combinations of cultivars and conditions. In medium-sized tomatoes, cuticular cracks’ onset occurs approximately 40 days after fruit set during the winter cultivation of ‘Calypso’ [27] and at the MG to breaker stage during the spring–summer cultivation of ‘The Amature’, ‘3120’, ‘Shugyoku’, and ‘San Marzano’ [26]. For large-sized beefsteak tomatoes, cuticular cracks was observed at 44 DAA during the summer–autumn cultivation of ‘Dombito’ [34] and two weeks after the fruit reached its maximum relative growth rate in the spring–autumn cultivation of ‘Rapsodie’ [16]. Although the rate of fruit development varied among cultivars and growth conditions—and these studies did not follow a unified criterion for defining the cuticular cracks onset—Dorais et al. [15] summarized the literature mentioning that cuticular cracks generally initiate at the beginning of the final phase of fruit growth. This phase is characterized by a decrease in skin elasticity, an increase in cell wall-degrading enzyme activity, and changes in cuticle composition [15]. However, under our cultivation conditions, the onset of cuticular cracks was observed at 20 DAA in both the summer–autumn cultivations, corresponding to the early-to-middle phase of fruit growth. In contrast, cuticular cracks first appeared at 30 DAA during the 2023 spring–summer cultivation, which corresponds to the MG to breaker stage. Our results indicate that, particularly in summer–autumn, fruits of ‘Nene’ become susceptible enough for the cuticular cracks onset at the immature to MG stage. Furthermore, the data clearly demonstrate that the stages susceptible to the cuticular cracks’ onset vary depending on the growth season.
Under our cultivation conditions, the onset of cuticular cracks occurred during the period of rapid fruit growth. The high growth strain on the fruit skin caused by rapid fruit enlargement can be assumed to increase its susceptibility to cuticular cracks. However, our results do not indicate that fruit growth or large fruit size alone promotes the onset of cuticular cracks in ‘Nene’. During the 2023 summer–autumn cultivation, fruit growth was delayed until after 20 DAA. As a result, changes in the fruit growth between 10 and 30 DAA were more similar between the 2022 summer–autumn and 2023 spring–summer cultivations than between the 2022 and 2023 summer–autumn cultivations. Nevertheless, the similarity in cuticular cracks’ frequency was more pronounced between the two summer–autumn seasons than between the 2022 summer–autumn and 2023 spring–summer cultivations. The comparison of fruit weight among cuticular crack severities showed that the weight of fruits with cuticular cracks was significantly higher than that of fruits without cuticular cracks only at 30 DAA in the 2023 spring–summer cultivation. From our results, we infer that while the onset of cuticular cracks in ‘Nene’ occurs during the stage when rapid fruit enlargement occurs, additional factors beyond rapid fruit enlargement contribute to this phenomenon.
One of the possible factors contributing to the cuticular cracks’ onset is the CM thickness. A significant increase in CM deposition was observed at 20 DAA in both the summer–autumn cultivations and at 30 DAA in the 2023 spring–summer cultivation (Figure 3). We also found that the CM deposition was greater in the fruits with cuticular cracks than in fruits without cuticular cracks at 30 DAA in the 2023 spring–summer cultivation (Table 1). Additionally, the CM deposition at 20 DAA was greater in both the summer–autumn cultivations, wherein approximately half of the fruits exhibited cuticular cracks, compared to that in the 2023 spring–summer cultivation, during which cuticular cracks were scarcely observed (Figure 3). The maximum strain of the CM is negatively correlated with its thickness [35]. In the MG stage, a thick CM in tomato fruits exhibited lower strain compared to a thin CM [36]. The relationship between the cuticular cracks’ onset and mechanical properties of the CM was reported by Kamimura et al. [26], who found that in the MG stage—during which cuticular cracks were initially observed in their study—the CM exhibited higher tensile strength and lower strain compared to that in younger stages. Based on previous studies, a thick CM exhibits reduced viscoelasticity and increased brittleness, making it more prone to failure. In our study, the susceptibility of CM to cuticular cracks’ onset may have peaked at 20 DAA in the summer–autumn cultivation and at 30 DAA in the spring–summer cultivation because of its thickness.
We further explored whether changes in the temperature or RH during the cultivation season contributed to the onset of cuticular cracks. Fruits exposed to high temperatures and low daily mean RH during the 2022 summer–autumn cultivation season tended to be more susceptible to CM failure. However, we could not identify similar relationships during the 2023 spring–summer and summer–autumn cultivation seasons. These results suggest that high temperatures may play some role in seasonal differences in the onset of cuticular cracks in ‘Nene’, which is consistent with previous findings [15]; however, attributing the presence or absence of cuticular cracks within the same growing season solely to temperature or RH is difficult, underscoring its limited impact. The involvement of additional environmental factors should also be considered, especially during the spring–summer cultivation. Factors, such as the light intensity [15,34] and CO2 enrichment [15], may also contribute to cuticular crack onset in ‘Nene’. The mechanical properties of the CM are also known to be influenced by its chemical composition [35]. For example, the components of the CM, such as cutin [37,38], epi-cuticular wax [39], polysaccharides [37,39], and flavonoids [40], influence its mechanical properties. These components undergo compositional changes during fruit growth [41,42,43,44]; for instance, flavonoids accumulate rapidly in the MG to red-ripe stage [40]. How these factors contribute to the occurrence of cuticular cracks in cherry tomatoes also warrants further investigation.

4.2. Progress of Cuticular Cracks Stages into Severe Net-like Forms

In tomato fruits, the absence of stomata results in water transpiration occurring primarily through the CM [1,2,18]. Consequently, a higher severity of cuticular cracks may result in more substantial economic losses. At 40 DAA, the frequency of grade 4 fruits was highest in the 2022 summer–autumn cultivation, followed by that in the 2023 summer–autumn and 2023 spring–summer cultivations (Figure 4). The onset of cuticular cracks was earlier in both the summer–autumn cultivations than in the 2023 spring–summer cultivation, indicating that early cuticular cracks’ onset in ‘Nene’ increases the final severity of cuticular cracks at harvest. This observation is consistent with previous findings that the incidence of severe cuticular cracks in fruit increases with the number of days between the cuticular cracks’ onset and harvest [16,27,28]. Bakker [27] conducted a nondestructive longitudinal study on cuticular cracks’ progression and reported that fruits with earlier cuticular cracks’ onset were more likely to progress to severe forms over time. Thus, the severity of cuticular cracks at harvest is closely related to its early onset, with an early onset increasing the likelihood of severe symptoms. Although the cuticular cracks’ severity at 20 DAA was comparable between the 2022 and 2023 summer–autumn cultivations, the progression of severity between 20–30 DAA was more pronounced in the 2022 summer–autumn cultivation. Among the parameters examined in this study, the most significant difference between the two summer–autumn cultivations was the fruit growth rate during 20–30 DAA, being 0.57 g∙day−1 in 2022 versus 0.20 g∙day−1 in 2023. The higher growth rate in 2022 may have contributed to the exacerbation of existing cuticular cracks.

5. Conclusions

The onset of cuticular cracks in the cherry tomato cultivar ‘Nene’ occurred at approximately 20 and 30 DAA in the summer–autumn and spring–summer cultivation, respectively. Differences in the temperature, relative humidity, and fruit growth within the cultivation season appeared to have limited effects on the onset of cuticular cracks. However, the severity of cuticular cracks at harvest was higher in the summer–autumn than in the spring–summer cultivation. In practice, cuticular cracks are usually recognized only when they become severe enough to result in the loss of gloss. Early-stage cuticular cracks are difficult to detect without microscopic observation but can potentially develop into severe cuticular cracks. Seasonal differences in the frequency of glossless fruits, as identified through visual inspection by farmers, may reflect variations in the stages most susceptible to the onset of cuticular cracks.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/horticulturae11010089/s1, Figure S1: Daily mean relative humidity during the cultivation period; Figure S2: Relationship between the cuticular cracks’ incidence and daily mean relative humidity (RH) from anthesis to the onset of cuticular cracks; Figure S3: Comparison of mean daily maximum temperature between fruits with cuticular cracks and without cuticular cracks from anthesis to the onset of cuticular cracks; Figure S4: Comparison of daily minimum temperature between fruits with cuticular cracks and without cuticular cracks from anthesis to the onset of cuticular cracks; Figure S5: Comparison of daily mean temperature between fruits with cuticular cracks and without cuticular cracks from anthesis to the onset of cuticular cracks; Figure S6: Comparison of mean daytime temperature between fruits with cuticular cracks and without cuticular cracks from anthesis to the onset of cuticular cracks; Figure S7: Comparison of mean nighttime temperature between fruits with cuticular cracks and without cuticular cracks from anthesis to the onset of cuticular cracks; Figure S8: Comparison of difference between daytime and nighttime temperatures between fruits with cuticular cracks and without cuticular cracks from anthesis to the onset of cuticular cracks; Figure S9: Comparison of daily mean relative humidity (RH) between fruits with cuticular cracks and without cuticular cracks from anthesis to the onset of cuticular cracks; Table S1: Analysis of fruit height, diameter, and length-to-width ratio in developing ‘Nene’ fruits classified by cuticular crack’ severity and cultivation season.

Author Contributions

R.H. designed the work, collected samples, conducted experiments, analyzed the data, and drafted the manuscript. K.I. reviewed and edited the manuscript. T.N. (Takashi Nishizawa) reviewed and edited the manuscript. T.N. (Tomoyuki Nabeshima) analyzed the data, supervised and edited the manuscript, and conducted project administration. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Data are contained within the article and Supplementary Materials.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Severity of cuticular cracks. (A): Grade 0 (fruits without cuticular cracks). (B): grade 1 (fruits with cuticular cracks, approximately <300 µm in length, with most cuticular cracks not connected to each other). (C): grade 2 (fruits with cuticular cracks, having a maximum length of approximately >300 µm, with half of cuticular cracks not connected to each other). (D): grade 3 (fruits with cuticular cracks connected to each other, with approximately half of the field of view covered with connected cuticular cracks). (E): grade 4 (fruits with cuticular cracks, forming a net-like structure, with almost the entire fruit surface under view covered with cuticular cracks).
Figure 1. Severity of cuticular cracks. (A): Grade 0 (fruits without cuticular cracks). (B): grade 1 (fruits with cuticular cracks, approximately <300 µm in length, with most cuticular cracks not connected to each other). (C): grade 2 (fruits with cuticular cracks, having a maximum length of approximately >300 µm, with half of cuticular cracks not connected to each other). (D): grade 3 (fruits with cuticular cracks connected to each other, with approximately half of the field of view covered with connected cuticular cracks). (E): grade 4 (fruits with cuticular cracks, forming a net-like structure, with almost the entire fruit surface under view covered with cuticular cracks).
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Figure 2. Daily mean temperature during the cultivation period. (A): 2023 spring–summer cultivation. (B): 2022 (solid line) and 2023 (dotted line) summer–autumn cultivations.
Figure 2. Daily mean temperature during the cultivation period. (A): 2023 spring–summer cultivation. (B): 2022 (solid line) and 2023 (dotted line) summer–autumn cultivations.
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Figure 3. Time–course of changes in fruit weight and cuticular membrane (CM) deposition classified by cultivation season. Values are expressed as the mean ± SE. (A): Fruit weight (n = 67–111). (B): CM deposition (n = 35–71). The open circle indicates the 2022 summer–autumn cultivation, the filled triangle indicates the 2023 spring–summer cultivation, and the filled circle indicates the 2023 summer–autumn cultivation. Different letters indicate significant differences between cultivation seasons using Tukey’s honestly significant difference test (p < 0.05).
Figure 3. Time–course of changes in fruit weight and cuticular membrane (CM) deposition classified by cultivation season. Values are expressed as the mean ± SE. (A): Fruit weight (n = 67–111). (B): CM deposition (n = 35–71). The open circle indicates the 2022 summer–autumn cultivation, the filled triangle indicates the 2023 spring–summer cultivation, and the filled circle indicates the 2023 summer–autumn cultivation. Different letters indicate significant differences between cultivation seasons using Tukey’s honestly significant difference test (p < 0.05).
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Figure 4. Time–course of changes in cuticular cracks’ severity incidence in developing ‘Nene’ fruits classified by cultivation season. Grade 0 (fruits without cuticular cracks). Grade 1 (fruits with cuticular cracks, approximately <300 µm in length, with most cuticular cracks not connected to each other). Grade 2 (fruits with cuticular cracks, having a maximum length of approximately >300 µm, with half of cuticular cracks not connected to each other). Grade 3 (fruits with cuticular cracks connected to each other, with approximately half of the field of view covered with connected cuticular cracks). Grade 4 (fruits with cuticular cracks, forming a net-like structure, with almost the entire fruit surface under view covered with cuticular cracks).
Figure 4. Time–course of changes in cuticular cracks’ severity incidence in developing ‘Nene’ fruits classified by cultivation season. Grade 0 (fruits without cuticular cracks). Grade 1 (fruits with cuticular cracks, approximately <300 µm in length, with most cuticular cracks not connected to each other). Grade 2 (fruits with cuticular cracks, having a maximum length of approximately >300 µm, with half of cuticular cracks not connected to each other). Grade 3 (fruits with cuticular cracks connected to each other, with approximately half of the field of view covered with connected cuticular cracks). Grade 4 (fruits with cuticular cracks, forming a net-like structure, with almost the entire fruit surface under view covered with cuticular cracks).
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Figure 5. Relationship between the cuticular cracks’ incidence and daily mean temperature from anthesis to the onset of cuticular cracks. Filled circles indicate the incidence of cuticular cracks, and open squares indicate the daily mean temperature. The incidence of cuticular cracks was calculated as the sum of fruits with grade 1, grade 2, grade 3, and grade 4 divided by the total number of fruits on the anthesis date. (A): 2022 summer cultivation (n = 106). Daily mean temperature was calculated over 20 days following anthesis. The incidence of cuticular cracks on 5 and 19 September was not recorded due to the absence of blooming flowers. (B): 2023 spring cultivation (n = 79). Daily mean temperature was calculated over 30 days following anthesis. The incidence of cuticular cracks on 7, 9, 24, and 25 May was not recorded due to the absence of blooming flowers. (C): 2023 summer cultivation (n = 67). Daily mean temperature was calculated over 20 days following anthesis. The incidence of cuticular cracks on 4 September was not recorded due to the absence of blooming flowers.
Figure 5. Relationship between the cuticular cracks’ incidence and daily mean temperature from anthesis to the onset of cuticular cracks. Filled circles indicate the incidence of cuticular cracks, and open squares indicate the daily mean temperature. The incidence of cuticular cracks was calculated as the sum of fruits with grade 1, grade 2, grade 3, and grade 4 divided by the total number of fruits on the anthesis date. (A): 2022 summer cultivation (n = 106). Daily mean temperature was calculated over 20 days following anthesis. The incidence of cuticular cracks on 5 and 19 September was not recorded due to the absence of blooming flowers. (B): 2023 spring cultivation (n = 79). Daily mean temperature was calculated over 30 days following anthesis. The incidence of cuticular cracks on 7, 9, 24, and 25 May was not recorded due to the absence of blooming flowers. (C): 2023 summer cultivation (n = 67). Daily mean temperature was calculated over 20 days following anthesis. The incidence of cuticular cracks on 4 September was not recorded due to the absence of blooming flowers.
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Figure 6. Comparison of accumulated temperature between fruits with cuticular cracks and without cuticular cracks from anthesis to the onset of cuticular cracks. The accumulated temperature was calculated as the sum of the daily mean temperatures over 20 (2022 and 2023 summer–autumn cultivations) or 30 (2023 spring–summer cultivation) days following anthesis. ** indicates a significant difference (p < 0.01), and n.s. indicates no significant difference between fruits with cuticular cracks and without cuticular cracks by t-test. (A): 2022 and 2023 summer–autumn cultivations. n = 32–53. (B): 2023 spring–autumn cultivation. n = 27 (fruits with cuticular cracks) and 52 (fruits without cuticular cracks).
Figure 6. Comparison of accumulated temperature between fruits with cuticular cracks and without cuticular cracks from anthesis to the onset of cuticular cracks. The accumulated temperature was calculated as the sum of the daily mean temperatures over 20 (2022 and 2023 summer–autumn cultivations) or 30 (2023 spring–summer cultivation) days following anthesis. ** indicates a significant difference (p < 0.01), and n.s. indicates no significant difference between fruits with cuticular cracks and without cuticular cracks by t-test. (A): 2022 and 2023 summer–autumn cultivations. n = 32–53. (B): 2023 spring–autumn cultivation. n = 27 (fruits with cuticular cracks) and 52 (fruits without cuticular cracks).
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Table 1. Analysis on fruit weight and cuticular membrane (CM) deposition in developing ‘Nene’ fruits classified by cuticular cracks’ severity and cultivation season.
Table 1. Analysis on fruit weight and cuticular membrane (CM) deposition in developing ‘Nene’ fruits classified by cuticular cracks’ severity and cultivation season.
DAACuticular Cracks’ Severity zFruit Weight (g) yCM Deposition (mg·cm−2) y
2022 Summer–Autumn2023 Spring–Summer2023 Summer–Autumn2022 Summer–Autumn2023 Spring–Summer x2023 Summer–Autumn
10Grade 04.42 ± 0.121.57 ± 0.093.55 ± 0.100.88 ± 0.03N.D.0.98 ± 0.03
Grade 15.41N.D.N.D.1.11N.D.N.D.
Grade 2N.D.N.D.N.D.N.D.N.D.N.D.
Grade 3N.D.N.D.N.D.N.D.N.D.N.D.
Grade 4N.D.N.D.N.D.N.D.N.D.N.D.
20Grade 011.90 ± 0.26 a10.81 ± 0.2411.25 ± 0.35 a1.96 ± 0.04 a1.60 ± 0.032.08 ± 0.02 a
Grade 112.32 ± 0.31 a11.1111.44 ± 0.36 a2.06 ± 0.03 a1.722.10 ± 0.03 a
Grade 212.11 ± 0.65 aN.D.10.59 ± 0.16 aN.D.N.D.2.20 ± 0.24 a
Grade 3N.D.N.D.N.D.N.D.N.D.N.D.
Grade 4N.D.N.D.N.D.N.D.N.D.N.D.
30Grade 0N.D.17.51 ± 0.29 b9.91N.D.2.68 ± 0.03 b1.65
Grade 117.01 ± 0.46 a19.65 ± 0.38 a13.18 ± 0.38 a2.06 ± 0.07 a2.87 ± 0.07 a2.01 ± 0.04 b
Grade 218.22 ± 0.59 a18.5713.43 ± 0.48 a2.15 ± 0.09 a18.572.19 ± 0.06 ab
Grade 317.85 ± 0.38 aN.D.13.81 ± 0.60 a2.05 ± 0.06 aN.D.2.28 ± 0.03 a
Grade 417.87 ± 0.74 aN.D.12.82 ± 0.63 a1.98N.D.2.37 ± 0.10 a
40Grade 0N.D.18.17 ± 0.39 a9.60N.D.2.61 ± 0.03 a2.25
Grade 121.69 ± 1.91 ab19.15 ± 0.35 a15.38 ± 0.76 a2.00 ± 0.09 b2.62 ± 0.03 a2.18 ± 0.06 a
Grade 222.08 ± 1.15 a19.46 ± 0.69 a16.17 ± 0.64 a2.22 ± 0.05 b2.52 ± 0.05 a2.21 ± 0.05 a
Grade 319.58 ± 0.43 ab20.3217.57 ± 0.98 a2.34 ± 0.04 abN.D.2.29 ± 0.07 a
Grade 418.70 ± 0.39 b16.78 ± 3.10 a16.95 ± 0.68 a2.50 ± 0.06 a2.79 ± 0.11 a2.39 ± 0.07 a
DAA: days after anthesis; N.D.: no data. z Grade 0 (fruits without cuticular cracks). Grade 1 (fruits with cuticular cracks, approximately <300 µm in length, with most cuticular cracks not connected to each other). Grade 2 (fruits with cuticular cracks, having a maximum length of approximately >300 µm, with half of cuticular cracks not connected to each other). Grade 3 (fruits with cuticular cracks connected to each other, with approximately half of the field of view covered with connected cuticular cracks). Grade 4 (fruits with cuticular cracks, forming a net-like structure, with almost the entire fruit surface under view covered with cuticular cracks). y Values are expressed as the mean ± SE. Different letters indicate significant differences between cuticular cracks’ severities by Tukey’s honestly significant difference test (p < 0.05). If only one sample was available for a given severity, it was excluded from statistical analysis. x At 10 DAA, CM deposition could not be determined because of insufficient CM thickness for isolation.
Table 2. Comparison of epidermal cell density in developing ‘Nene’ fruits between fruits with cuticular cracks and without cuticular cracks.
Table 2. Comparison of epidermal cell density in developing ‘Nene’ fruits between fruits with cuticular cracks and without cuticular cracks.
Cultivation SeasonDAACuticular Cracks’ OccurrencenzEpidermal Cell Density (Number/Observed Area (275.53 µm × 206.65 µm)) y
2022 summer–autumn20Without cuticular cracks2142.26 ± 2.03n.s.
With cuticular cracks3139.35 ± 1.10
2023 spring–summer30Without cuticular cracks543.88 ± 4.44n.s.
With cuticular cracks538.08 ± 3.27
40Without cuticular cracks537.20 ± 2.79n.s.
With cuticular cracks537.38 ± 3.38
2023 summer–autumn20Without cuticular cracks535.65 ± 2.13n.s.
With cuticular cracks533.70 ± 3.20
DAA: days after anthesis. z Number of replicates. y Values are expressed as the mean ± SE. n.s. indicates no significant difference between fruits with cuticular cracks and without cuticular cracks by t-test (p < 0.05).
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Hosoi, R.; Ikeda, K.; Nishizawa, T.; Nabeshima, T. Time–Course Analysis of the Onset and Progression of Cuticle Cracking in Fruits of Cherry Tomato Cultivar ‘Nene’. Horticulturae 2025, 11, 89. https://doi.org/10.3390/horticulturae11010089

AMA Style

Hosoi R, Ikeda K, Nishizawa T, Nabeshima T. Time–Course Analysis of the Onset and Progression of Cuticle Cracking in Fruits of Cherry Tomato Cultivar ‘Nene’. Horticulturae. 2025; 11(1):89. https://doi.org/10.3390/horticulturae11010089

Chicago/Turabian Style

Hosoi, Ryosuke, Kazuo Ikeda, Takashi Nishizawa, and Tomoyuki Nabeshima. 2025. "Time–Course Analysis of the Onset and Progression of Cuticle Cracking in Fruits of Cherry Tomato Cultivar ‘Nene’" Horticulturae 11, no. 1: 89. https://doi.org/10.3390/horticulturae11010089

APA Style

Hosoi, R., Ikeda, K., Nishizawa, T., & Nabeshima, T. (2025). Time–Course Analysis of the Onset and Progression of Cuticle Cracking in Fruits of Cherry Tomato Cultivar ‘Nene’. Horticulturae, 11(1), 89. https://doi.org/10.3390/horticulturae11010089

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