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Article

Effects of Endogenous Melatonin Deficiency on the Growth, Productivity, and Fruit Quality Properties of Tomato Plants

by
Zhuo He
1,
Cen Wen
1 and
Wen Xu
1,2,*
1
College of Agriculture, Guizhou University, Guiyang 550025, China
2
Engineering Research Center for Protected Vegetable Crops in Higher Learning Institutions of Guizhou Province, Guiyang 550025, China
*
Author to whom correspondence should be addressed.
Horticulturae 2023, 9(8), 851; https://doi.org/10.3390/horticulturae9080851
Submission received: 16 June 2023 / Revised: 18 July 2023 / Accepted: 24 July 2023 / Published: 26 July 2023
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Abstract

:
Caffeic acid O-methyltransferase 1 (COMT1) is a key enzyme that is involved in melatonin synthesis, affecting the melatonin content in plants. In this experiment, tomato plants (slcomt1) with silenced SlCOMT1 gene expression were used to investigate the effects of SlCOMT1 deficiency on fruit growth, development, and quality formation. The results show that the slcomt1 plants exhibited prolonged fruit development, with reductions in the relative expression levels of SlCOMT1 by 71.1%, 79.7%, 83.9%, and 90.6% during the green fruit, breaker, orange ripening, and red ripening stages, respectively. The endogenous melatonin content also decreased by 29.4%, 43%, 45%, and 61.4% in the corresponding stages. Furthermore, the slcomt1 plants showed a decrease in the individual fruit weight, seed number per fruit, and fruit set rate by approximately 51.1%, 48.2%, and 30.4%, respectively. The slcomt1 plants exhibited an increase in the titratable acid content by 32.1%, 22.1%, 10.3%, and 24.4% during the green fruit, breaker, orange ripening, and red ripening stages, while the sugar-to-acid ratio decreased by 44.9%, 32.6%, 22.7%, and 36.8%. The slcomt1 plants also displayed increased fruit firmness, along with reductions in the relative expression levels of the cell wall and carotenoid-related genes and carotenoid content. Specifically, the Vc content in the slcomt1 plants decreased by 80.7% during the green fruit stage, and by 11.5%, 17.1%, and 2.6% during the breaker, orange ripening, and red ripening stages, respectively. The soluble protein content exhibited a decreasing trend in the corresponding stages. This study highlights the important role of endogenous melatonin in fruit physiology and quality formation, providing insights for further research and application of melatonin in agriculture.

1. Introduction

Tomato (Solanum lycopersicum L.) is native to South America. It was introduced to Europe in the 16th century and later reached China in the 17th century [1]. Tomato belongs to the Solanaceae family and is an annual or perennial herbaceous plant. It is widely cultivated as a major vegetable crop in countries around the world and ranks among the top ten most consumed vegetables [2]. With the improvement of living standards and increased health consciousness, consumers are paying more attention to the quality of tomato fruits, including their appearance, nutritional value, flavor, and color. High-quality vegetables require excellent flavor, desirable marketable characteristics, and high nutritional value [3]. Tomatoes are rich in various mineral elements such as vitamins B2 and C, fructose, proteins, as well as calcium, phosphorus, iron, and other essential minerals [4]. They also contain lycopene, which is a highly potent antioxidant from the carotenoid family [5]. Tomatoes are considered important fruiting crops with significant health benefits and nutritional value.
Melatonin (N-acetyl-5-methoxytryptamine) is an indole derivative of tryptophan. Upon its initial isolation, melatonin was named MT [6] due to its ability to reverse the darkening effect of the melanocyte-stimulating hormone. In 1995, the presence of melatonin was simultaneously discovered in vascular plants by two research groups [7,8]. Melatonin is found in various plant organs, including in the leaves, stems, roots, fruits, and seeds [9,10], and it is present in nearly all plant tissues [11,12]. Despite the relatively short history of the study of melatonin in plants, recent years have seen an increasing interest in understanding its role. Melatonin was shown to have various effects in plant physiology. It promotes lateral root and seedling growth while inhibiting primary root growth [13,14,15]. It enhances the quantum yield and photosynthetic efficiency of photosystem II [16]. Moreover, melatonin plays a role in delaying dark-induced leaf senescence [17,18]. Melatonin was also found to have beneficial effects on plant responses to environmental stresses. It improves cold tolerance and reduces flavor and nutritional losses caused by chilling injury [19,20]. Under heat stress, melatonin increases endogenous melatonin levels, mitigating heat-stress-induced damage [21,22]. It protects chlorophyll and enhances drought tolerance [23,24,25]. Furthermore, melatonin enhances salt tolerance in many plant species [26,27,28], and its levels increase in plants under waterlogging stress [29,30]. Melatonin treatment was also shown to alleviate heavy metal inhibition on growth [31,32,33] and enhance tomato resistance to pathogenic Phytophthora infestans as well as enhance cherry tomato tolerance [34,35]. These extensive applications of melatonin in agriculture underscore its significant role. However, there is limited research on the involvement of endogenous melatonin in the growth, development, and quality formation of tomato fruits. Further investigation is needed to explore the specific mechanisms through which endogenous melatonin influences these processes.
The synthesis of melatonin in plants is primarily mediated by six different enzymes, including tryptophan decarboxylase (TDC), tryptophan hydroxylase (TPH), tryptamine 5-hydroxylase (T5H), serotonin N-acetyltransferase (SNAT), acetylserotonin methyl transferase (ASMT), and caffeic acid O-methyltransferase (COMT) [36]. Byeon et al.’s study [37] revealed that COMT and ASMT belong to the O-methyltransferase family and are capable of methylating phenylpropanoid compounds, flavonoids, and alkaloids. The COMT enzyme, which is specifically involved in the methylation of N-acetylserotonin, was renamed as COMT1. The experimental materials for this study consisted of SlCOMT1 gene-silenced tomato plants obtained through the gene editing technique of Crispr/Cas9 by the researcher Ye Xinyue, who is a member of the project team [38]; the differences in fruit growth and development as well as quality formation were investigated between the silenced SlCOMT1 plants and the wild-type plants. This research aims to provide a theoretical foundation for understanding the physiological mechanisms underlying the regulation of fruit growth, development, and quality formation by the SlCOMT1 gene, as well as the application of melatonin. It contributes to a deeper understanding of the regulatory mechanisms of melatonin in tomato fruit growth and development, ultimately leading to an improved tomato yield and quality.

2. Materials and Methods

2.1. Experimental Materials

The experiment was conducted in the laboratory of the Department of Horticulture, College of Agriculture, Guizhou University. The experimental materials for this study included “Micro-Tom” tomato plants, which were self-pollinated and maintained by our research team, serving as the wild-type control (WT). In addition, SlCOMT1 single-gene silenced plants (slcomt1) were generated and validated using the Crispr/Cas9 gene editing technique by our team member, Ye Xinyue. The disinfected tomato seeds were subjected to pre-germination, and once the radicle emerged, they were sown in a controlled environment chamber with a photoperiod of 18 h of light and 6 h of darkness at 25 °C. After the seedlings reached the three-leaf stage, they were transplanted for daily management.

2.2. Experimental Methods

2.2.1. Assessment of Fruit Hardness

Fruit hardness was measured using a GY-4 type fruit hardness (Fangke Shandong, China) tester. Prior to measurement, the gauge was adjusted to 0 by aligning the first tick mark on the dial with the drive pointer. During measurement, the fruit hardness tester was gripped and pressed uniformly and vertically into the tomato fruit. The data indicated by the probe were observed, and once the probe reached 10 mm, further penetration into the fruit was stopped. The reading indicated by the pointer was recorded as the hardness of the tomato fruit. After measurement, the knob was rotated to return the pointer to the initial tick mark at zero. Nine biological replicates, each consisting of three technical replicates, were established for both the WT and slcomt1 fruits.

2.2.2. Determination of Tomato Lycopene and Carotenoid Content

The determination of tomato lycopene content was conducted following the method described by Sun et al. [39]. The results are expressed as milligrams of lycopene per kilogram (mg·kg−1) based on fresh weight. The determination of carotenoid content was conducted using the Plant Carotenoid Content Detection Kit (Solarbo Beijing, Beijing, China). Each tissue sample was assessed using three biological replicates.

2.2.3. Determination of Ascorbic Acid Content

Tissues weighing 0.5 g to 10 mg were taken and pre-rinsed in pre-chilled PBS, followed by blotting with filter paper and accurate weighing of 0.2 g of tissue. The supernatant was collected and analyzed for vitamin C (VC)/ascorbic acid (ASA) content following the instructions provided in the kit manual of the Nanjing Jiancheng Institute of Biotechnology Vitamin C/Ascorbic Acid Assay Kit. Each tissue sample had three biological replicates.

2.2.4. Determination of Soluble Solid Content, Titratable Acid Content, and Sugar-to-Acid Ratio

The determination of fruit soluble solid content (SSC%) and titratable acid content (TA%) was performed using a PAL-BX/ACD1 refractometer (ATAGO, Tokyo, Japan). The sugar-to-acid ratio (SAR) was calculated as SSC/TA.

2.2.5. Analysis of Tomato Agronomic Traits

WT and slcomt1 plants were photographed to compare fruit and cross-section phenotypes at 5 d, 10 d, 15 d, 20 d, 25 d, 30 d, 35 d, 40 d, and 45 d after flowering. The fruit set rate was determined by observing the development of flower buds from the tetrad stage of stamen development to mature fruits in the WT and slcomt1 plants. The fruit set rate was calculated for the same flower clusters during the corresponding time periods. Fruit set rate is defined as the percentage (%) of actual fruit count in relation to the total number of flowers. Twelve plants were evaluated for each sample. The formula used to calculate the fruit set rate is as follows: fruit set rate = (fruit count/flower count) × 100%. Additionally, for the WT and slcomt1 fruits, thirty fully mature fruits were randomly selected and the number of seeds per fruit was counted. The weight of each individual fruit was measured.

2.2.6. Determination of Endogenous Melatonin Content

Samples of 0.3 g of different tomato tissues were weighed and mixed with 3 mL of phosphate-buffered solution. The mixture was homogenized on ice and centrifuged at 3000 rpm for 10 min to collect the supernatant. The endogenous melatonin content in different tissues was determined following the instructions provided in the Plant MTELISA assay kit (Yuanju, Shanghai, China), and three biological replicates were performed for each tissue.

2.2.7. RNA Isolation and Quantitative Real-Time PCR

The extraction of total RNA from tomato fruits was performed using a commercial kit (DP432, Shanghai Tiangen, Shanghai, China). The extraction procedure was carried out according to the instructions provided with the kit. The purity and concentration of RNA were assessed using gel electrophoresis and a B-500 micro-volume spectrophotometer (Yuanxi, Shanghai, China). The total RNA (2 μL) was reverse transcribed into cDNA using a first-strand cDNA synthesis kit (KR118, Tiangen, Shanghai, China), and the resulting cDNA was stored at −20 °C for further use. Fluorescent quantitative PCR (qRT-PCR) was performed using SYBR-Green dye on the FQD1-96A instrument (BIOER, Hangzhou, China). The reaction mixture (20 μL) consisted of 2 μL cDNA template, 10 μL 2× SYBR-Green MIX, 6.8 μL RNase-Free ddH2O, 0.6 μL of the forward primer, and 0.6 μL of the reverse primer. The PCR program included an initial denaturation step at 95 °C for 3 min, followed by 40 cycles of three-step amplification, including 95 °C for 5 s, 60 °C for 30 s, and 72 °C for 15 s, with fluorescence signal collection. The melt curve stage started at 60 °C for 30 s and increased to 95 °C with a 0.5 °C increment every 30 s to generate a melt curve. The reference gene used was tomato Actin (Solyc03g078400). Each treatment was performed with three biological replicates, and each biological replicate had three technical replicates. See “Supplementary Table S1” for qRT-PCR primers. The relative gene expression was calculated using the 2−ΔΔCt method [40].

2.3. Data Processing and Analysis

The measured values were calculated using Microsoft Excel 2019. The significance of the results was analyzed using SPSS Statistics 23.0, and multiple comparisons were performed using Duncan’s method. Different lowercase letters in the figure indicate significant differences (p < 0.05). Graphs were generated using GraphPad Prism 8.0.2 software, and the data are presented as mean ± standard deviation.

3. Results

3.1. The Effects of SlCOMT1 Gene Deficiency on Endogenous Melatonin Content and Fruit Phenotype and Ventricle

To investigate the influence of endogenous melatonin on the growth and development of tomato fruits, we silenced the SlCOMT1 gene, which is involved in melatonin biosynthesis. As shown in Figure 1A, compared to wild-type tomato plants, the melatonin levels in the slcomt1 fruits decreased by 29.4%, 43%, 45%, and 61.4% during the green fruit, breaker, orange ripening, and red ripening stages, respectively. Additionally, the relative expression levels of SlCOMT1 in the fruits of slcomt1 at corresponding stages were reduced by 72.6%, 79.7%, 83.9%, and 90.6% (Figure 1B). Consequently, we observed the phenotypic changes during the maturation process of the tomato fruits. While the WT tomato fruits entered the orange ripening stage at 35 days, the slcomt1 fruits were still in the breaker stage and lagged behind the WT fruits. Upon fruit sectioning, it was evident that the gel development in the slcomt1 fruits occurred later than in the WT fruits, and the gel in the WT fruits appeared fuller and exhibited a wider liquefaction range compared to the slcomt1 fruits (Figure 1C). Thus, the SlCOMT1 resulted in a reduction in the endogenous melatonin biosynthesis and affected the growth and development of the tomato fruits.

3.2. Impact of SlCOMT1 Gene Deficiency on Fruit Development

In order to elucidate the influence of melatonin on fruit development, we conducted observations on fully matured fruits and discovered a significant reduction in the seed count within the slcomt1 fruits compared to the WT fruits (Figure 2A). Moreover, when compared to the WT tomato plants, the slcomt1 fruits exhibited an approximate decrease of 51.1% in the individual fruit weight (Figure 2B), a reduction of about 48.2% in the seed count per fruit (Figure 2C), and a decline in the fruit set rate of approximately 30.4% (Figure 2D). These findings indicate that the SlCOMT1 gene plays a significant role in tomato fruit development, as the decrease in the endogenous melatonin content notably diminishes the fruit yield.

3.3. Impact of SlCOMT1 Gene Deficiency on Fruit Color Formation

To further investigate the influence of endogenous melatonin on the tomato fruit color formation, we conducted analyses of the carotenoid content and key genes involved in their synthesis at four developmental stages of both the WT and slcomt1 fruits. The experimental results reveal that as the fruits matured, the levels of lycopene and carotenoids gradually increased. Compared to the WT fruits, the slcomt1 fruits exhibited a reduction of 39.9%, 47.3%, 34.5%, and 26.8% in the lycopene content during the green fruit stage, breaker stage, orange ripening stage, and red ripening stage, respectively. Similarly, the carotenoid content also showed a decrease of 25.5%, 32.3%, 21.4%, and 18.9% (Figure 3A,B). The expression levels of SlCRTISO, SlPSY1, SlZDS, SlDXR, SlGGPS2, and SlPDS in the slcomt1 fruits were downregulated to varying degrees compared to the WT fruits. Although SlCRTISO and SlPSY1 showed higher expression levels in the WT fruits across the four stages of fruit ripening, their expression levels gradually declined as the fruits matured (Figure 3C,D). The maximum accumulation of lycopene and carotenoids occurred during the red ripening stage, while the expression levels of the carotenoid-synthesis-related genes (SlZDS, SlDXR, SlGGPS2, SlPDS) peaked during the orange ripening stage (Figure 3E–H). This suggests that the substantial accumulation of lycopene and carotenoids during the red ripening stage may be attributed to the high expression of key synthesis-related genes during the orange ripening stage. These findings indicate that endogenous melatonin may enhance the lycopene content in tomato fruits and affect the conversion of lycopene to carotenoids by modulating the expression of carotenoid-synthesis-related genes, ultimately influencing the color formation of tomato fruits.

3.4. Impact of SlCOMT1 Gene Deficiency on Fruit Texture

Subsequently, to investigate the role of endogenous melatonin in tomato fruit texture, we conducted measurements of fruit firmness. The results reveal that the slcomt1 fruits exhibited significantly higher firmness than the WT fruits across all four stages (Figure 4A). In order to gain a comprehensive understanding of the influence of endogenous melatonin on the cell wall structure, the relative expression levels of five genes (SlEXP1, SlPE1, SlPG2A, SlTBG4, SlXTHS) that are associated with the cell wall structure in tomato fruit were determined at four developmental stages (Figure 4B–F). This suggests that endogenous melatonin may participate in the fruit softening process by regulating the genes associated with the cell wall structure.

3.5. Impact of SlCOMT1 Gene Deficiency on Fruit Flavor

Following that, we investigated the impact of endogenous melatonin on the flavor of tomato fruits by measuring the soluble solids content, titratable acidity, and the sugar-to-acid ratio. The results demonstrate that the slcomt1 fruits exhibited significant reductions of 27.3%, 17.7%, 14.7%, and 21.5% in the soluble solids content during the green fruit stage, breaker stage, orange ripening stage, and red ripening stage, respectively, compared to the WT fruits (Figure 5A). Furthermore, the titratable acid content significantly increased by 32.1% in the slcomt1 fruits during the green fruit stage, increased by 22.1% during the breaker stage, and significantly rose by 10.3% and 24.4% during the orange ripening stage and red ripening stage, respectively (Figure 5B). The sugar-to-acid ratio in the slcomt1 fruits exhibited significant decreases of 44.9% and 32.6% during the green fruit stage and breaker stage, respectively, while it also decreased by 22.7% and 36.8% during the orange ripening stage and red ripening stage, respectively (Figure 5C). These findings suggest that the silencing of the SlCOMT1 gene leads to reduced fruit palatability, and endogenous melatonin may play a crucial role in the development of the characteristic “tomato taste”.

3.6. Impact of SlCOMT1 Gene Deficiency on Fruit Nutrient Composition

Finally, we investigated the effect of endogenous melatonin on the levels of vitamin C (Vc) and soluble proteins in tomato fruits. Our findings reveal that during the green fruit stage, the soluble protein content in the slcomt1 fruits was significantly lower than that in the WT fruits by 46%. Furthermore, in the stages of breaker, orange ripening, and red ripening, the soluble protein content in the comt1 fruits exhibited respective decreases of 6.9%, 9.2%, and 17.4% (Figure 6A). Similarly, The Vc content in the slcomt1 fruits was significantly lower than that in the WT fruits during the green fruit, breaker, orange ripening, and red ripening stages, with reductions of 80.7%, 11.5%, 17.1%, and 2.6%, respectively (Figure 6B). These results indicate that endogenous melatonin plays a significant role in the formation of nutrient components in tomato fruits.

4. Discussion

The presence of melatonin in tomato fruits was first detected in 1995 in currant tomatoes [8]. In general, when multiple substrates coexist within a cell, a substrate can act as a competitive inhibitor for the enzymatic catalysis of another substrate, depending on the differential affinity of the enzyme for each substrate [41]. The optimal substrates for AtCOMT1 were found to be 5-hydroxyconiferaldehyde (Km = 12.7 μM), followed by caffeic acid (Km = 103 μM), and finally, NAS (Km = 233 μM). Additionally, AtCOMT exhibited a dose-dependent inhibition of NAS methylation by caffeic acid [37]. Due to the abundance of caffeic acid and its derivatives in plant cells, in rice, a reverse reaction for the biosynthesis of melatonin, mediated by N-acetylserotonin deacetylase (ASDAC), converts N-acetylserotonin (NAS) into serotonin, thus controlling the balance of endogenous melatonin [42]. Ahmmed et al. observed a 70% decrease in expression level and an 86% reduction in endogenous melatonin content when SlCOMT1 was silenced [21]. In this study, during the four stages of tomato fruit development, the expression of slcomt1 in the fruit was significantly downregulated by 72.6%, 79.7%, 83.9%, and 90.6%, respectively, paralleled by a corresponding decrease in the endogenous melatonin content by 29.4%, 43%, 45%, and 61.4%. These findings are consistent with those from the research conducted by Ahmmed et al., indicating a close correlation between the expression of the SlCOMT1 gene and the biosynthesis of endogenous melatonin during tomato fruit development.
During the process of fruit development and ripening, the change in color from green to red is a result of carotenoid accumulation and chlorophyll degradation. Lycopene is the most abundant carotenoid in tomato fruit, and it serves as a precursor for the synthesis of vitamin A and functions as a potent antioxidant. It plays a crucial role in human nutrition and health [43,44]. The biosynthesis of lycopene in plants primarily occurs via the isoprenoid pathway. It begins with the conversion of geranylgeranyl pyrophosphate (GGPP) to phytoene, which is the precursor of lycopene. Subsequently, through four consecutive desaturation reactions, all-trans lycopene is produced [45]. The initial step in carotenoid synthesis is catalyzed by PSY1, a fruit-specific enzyme that is responsible for the synthesis of phytoene, which is the precursor of carotenoids. CRTISO, encoded by the CRTISO gene, functions as a carotene isomerase, facilitating the isomerization of cis lycopene to all-trans lycopene [46]. In this study, we observed that the levels of lycopene and carotenoids gradually increased during fruit ripening in both the slcomt1 and WT fruits. However, compared to the WT fruits, the slcomt1 fruits exhibited varying degrees of reduction in these contents. Furthermore, the expression levels of the genes associated with carotenoid synthesis, including SlCRTISO, SlPSY1, SlZDS, SlDXR, SlGGPS2, and SlPDS, also exhibited changes in the slcomt1 fruits, albeit with different trends. This may indicate that each gene plays a distinct role in carotenoid synthesis, and further investigation is required to elucidate the specific regulatory mechanisms involved. Our study revealed that endogenous melatonin plays a role in promoting lycopene accumulation during tomato fruit ripening, potentially affecting the transcription and translation levels of genes involved in carotenoid synthesis, in conjunction with other unknown mechanisms. Consequently, the delayed onset of color change in the slcomt1 tomato fruits compared to the WT fruits can be attributed to these combined effects. Additionally, Sun et al. found that exogenous melatonin treatment can enhance fruit ripening in tomatoes by upregulating ripening-related genes [39].
Fruit softening primarily occurs due to cell wall degradation and reduced cell adhesion, which are essential prerequisites for fruit edibility. The cell wall of the fruit is a complex network composed of polysaccharides and proteins [47]. Alterations in the cell wall structure lead to the gradual degradation of high-molecular-weight polymers within the cell wall and the loss of integrity in the pectin-rich middle lamella, resulting in reduced cell adhesion and subsequent fruit softening [48]. In this study, we observed a downregulation trend in the expression of the genes related to cell wall synthesis, including SlEXP1, SlPE1, SlPG2A, SlTBG4, and SlXTHS, during the four developmental stages of the slcomt1 fruits. Correspondingly, the fruit hardness at each stage exhibited an upward trend, with significant increases of 13.1%, 9.8%, 39%, and 32.3%, respectively. Ei-Naby et al. [49]. found that exogenous melatonin treatment improved the endogenous melatonin levels, resulting in increased apricot yield and fruit hardness. Therefore, it can be inferred that endogenous melatonin may also participate in the regulation of fruit texture changes.
Soluble solids include a series of substances such as soluble sugars and organic acids, and they are an important indicator for evaluating tomato flavor in field production due to their convenient measurement. Previous studies have demonstrated that an appropriate sugar-to-acid ratio is a key determinant of tomato flavor [50]. A desirable flavor profile requires a suitable sugar-to-acid ratio on the basis of a high sugar content. The optimal sugar-to-acid ratio is reported to be in the range of 6.9 to 10 [51], while some suggest a ratio of 4 to 6 [52]. In this study, the sugar-to-acid ratio of the slcomt1 fruits during the green fruit stage was only 1.1, and it reached 3.7 during the red ripening stage, whereas the WT fruits reached a ratio of 5.8 during the red ripening stage. The sugar-to-acid ratio at other stages was also significantly lower than that of the WT plants. Previous studies have reported that exogenous melatonin treatment increased the sugar-to-acid ratio in sweet cherries [53]. Therefore, endogenous melatonin may have a certain influence on the accumulation of soluble solids. However, further research is needed to investigate the specific mechanisms by which it regulates the flavor formation of tomato fruits.
VC, also known as ascorbic acid (AsA), is a hexose lactone compound. As a potent antioxidant, ascorbic acid plays a vital role in plant physiology by regulating cellular signaling pathways and acting as a co-factor in various physiological processes [54,55,56]. In addition to its crucial physiological and biochemical functions in plants, ascorbic acid is an important nutrient that helps humans to resist various diseases. Unlike plants, humans lack the final key enzyme (L-Gulino-1,4-lactone) in the ascorbic acid biosynthesis pathway, rendering them unable to synthesize ascorbic acid endogenously [57], and thus relying on dietary intake. The soluble protein content not only reflects the plant’s ability to withstand stress, but also indicates the level of proteinaceous nutrients in the fruit. In this study, the levels of both vitamin C (Vc) and soluble proteins in the slcomt1 fruits exhibited a decreasing trend during the four developmental stages. Previous studies have also reported that irrigation with melatonin (MT) enhanced the levels of soluble proteins in tomatoes under drought stress, while foliar application of melatonin increased the Vc content in tomatoes [58,59]. Therefore, endogenous melatonin plays a role in the accumulation of Vc and soluble proteins in tomato fruits. Combined with the results of other quality-related indicators, this indicates the involvement of endogenous melatonin in the regulation of tomato fruit growth, development, and quality formation. However, further research is needed to elucidate the specific regulatory mechanisms involved.

5. Conclusions

In this experiment, silencing the key melatonin synthesis gene SlCOMT1 resulted in reduced endogenous melatonin levels, significantly delaying the growth and development of tomato fruits and impairing fruit quality. It led to decreased fruit weight, number of seeds per fruit, levels of carotenoids, lycopene, soluble solids, vitamin C (Vc), and soluble proteins throughout the four stages of fruit development. Additionally, it increased the titratable acid content and downregulated genes involved in carotenoid synthesis (SlCRTISO, SlPSY1, SlZDS, SlDXR, SlGGPS2, SlPDS), as well as genes related to cell wall synthesis (SlEXP1, SlPE1, SlPG2A, SlTBG4, SlXTHS). Consequently, this study expands our understanding of the role of endogenous melatonin in promoting tomato fruit growth and development and provides evidence for its involvement in tomato fruit quality formation.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae9080851/s1, Table S1: qPCR sequence of differential genes in tomoto fruit.

Author Contributions

Z.H., conceptualization, writing—original draft, formal analysis, data curation, software, methodology, and validation. C.W., software and validation. W.X., writing—review and editing, conceptualization, funding acquisition, project administration, resources, and supervision. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (31760594 and 32260754).; the Special Project for Cultivating Innovative Talents of Thousand Levels in Guizhou Province ((2018)02), and the Guizhou University of Science and Technology Research Start-up Fund for New Faculty ((2016)48).

Data Availability Statement

The authors will supply the relevant data in response to reasonable requests.

Acknowledgments

The authors are grateful to the National and Local Vegetable Engineering Center (Guizhou) and the Laboratory of the Department of Horticulture (Agricultural College of Guizhou University) for their support in this project.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Observation of endogenous melatonin levels and fruit phenotypes. (A) Endogenous melatonin levels at four stages of tomato fruit development. Gr: green fruit stage, Br: breaker stage, Or: orange ripening stage, Re: red ripening stage, WT: wild-type plants, slcomt1: SlCOMT1 gene-silenced plants. (B) Relative expression levels of the SlCOMT1 gene. (C) Phenotypic observations and cross sections of fruits at 5 d, 10 d, 15 d, 20 d, 25 d, 30 d, 35 d, 40 d, and 45 d after flower opening. Bars = 1 cm. The data shown are the average of three replicates, and the error bars represent the standard deviation. The same letter indicates no significant difference at p < 0.05 (Duncan’s test).
Figure 1. Observation of endogenous melatonin levels and fruit phenotypes. (A) Endogenous melatonin levels at four stages of tomato fruit development. Gr: green fruit stage, Br: breaker stage, Or: orange ripening stage, Re: red ripening stage, WT: wild-type plants, slcomt1: SlCOMT1 gene-silenced plants. (B) Relative expression levels of the SlCOMT1 gene. (C) Phenotypic observations and cross sections of fruits at 5 d, 10 d, 15 d, 20 d, 25 d, 30 d, 35 d, 40 d, and 45 d after flower opening. Bars = 1 cm. The data shown are the average of three replicates, and the error bars represent the standard deviation. The same letter indicates no significant difference at p < 0.05 (Duncan’s test).
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Figure 2. Tomato fruit development and phenotypic characteristics of mature fruits, including cross sections. (A) Phenotypic characteristics and cross sections of ripe fruits. WT: wild-type plants, slcomt1: SlCOMT1 gene-silenced plants. (B) Individual fruit weight. The weight of thirty fruits was measured for each type, with six plants. (C) Number of seeds per fruit. The count was calculated for thirty fruits for each type, with six plants. (D) Fruit set rate. Data were collected from twelve plants. slcomt1-1, slcomt1-2, and slcomt1-3 are the three replicates of silenced plants of the SlCOMT1 gene. The presented data represent the mean values, and error bars represent the standard deviation. The same letter indicates no significant difference in mean values at p < 0.05 (Duncan’s test).
Figure 2. Tomato fruit development and phenotypic characteristics of mature fruits, including cross sections. (A) Phenotypic characteristics and cross sections of ripe fruits. WT: wild-type plants, slcomt1: SlCOMT1 gene-silenced plants. (B) Individual fruit weight. The weight of thirty fruits was measured for each type, with six plants. (C) Number of seeds per fruit. The count was calculated for thirty fruits for each type, with six plants. (D) Fruit set rate. Data were collected from twelve plants. slcomt1-1, slcomt1-2, and slcomt1-3 are the three replicates of silenced plants of the SlCOMT1 gene. The presented data represent the mean values, and error bars represent the standard deviation. The same letter indicates no significant difference in mean values at p < 0.05 (Duncan’s test).
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Figure 3. Carotenoid content and expression levels of key genes involved in carotenoid synthesis in tomato fruits. (A) Lycopene content at four developmental stages of tomato fruits. (B) Carotenoid content at four developmental stages of tomato fruits. (B–H) qRT-PCR analysis of the expression levels of carotenoid-synthesis-related genes, including SlCRTISO, SlPSY1, SlZDS, SlDXR, SlGGPS2, and SlPDS. The data shown are the mean values of three replicates, and the error bars represent the standard deviation. The same letter indicates no significant difference in mean values at p < 0.05 (Duncan’s test).
Figure 3. Carotenoid content and expression levels of key genes involved in carotenoid synthesis in tomato fruits. (A) Lycopene content at four developmental stages of tomato fruits. (B) Carotenoid content at four developmental stages of tomato fruits. (B–H) qRT-PCR analysis of the expression levels of carotenoid-synthesis-related genes, including SlCRTISO, SlPSY1, SlZDS, SlDXR, SlGGPS2, and SlPDS. The data shown are the mean values of three replicates, and the error bars represent the standard deviation. The same letter indicates no significant difference in mean values at p < 0.05 (Duncan’s test).
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Figure 4. Tomato fruit firmness and expression levels of genes related to cell wall synthesis. (A) Fruit firmness during four stages of tomato fruit development. (B–F) qRT-PCR analysis of the expression levels of cell-wall-related genes SlEXP1, SlPE1, SlPG2A, SlTBG4, and SlXTH. The presented data represent the average of three replicates, with error bars indicating the standard deviation. The same letter indicates no significant difference in mean values at p < 0.05 (Duncan’s test).
Figure 4. Tomato fruit firmness and expression levels of genes related to cell wall synthesis. (A) Fruit firmness during four stages of tomato fruit development. (B–F) qRT-PCR analysis of the expression levels of cell-wall-related genes SlEXP1, SlPE1, SlPG2A, SlTBG4, and SlXTH. The presented data represent the average of three replicates, with error bars indicating the standard deviation. The same letter indicates no significant difference in mean values at p < 0.05 (Duncan’s test).
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Figure 5. Contents of flavor-related compounds in tomato fruits. (A) Soluble solids content (SSC) during four stages of tomato fruit development. (B) Titratable acidity (TA) during four stages of tomato fruit development. (C) Sugar-to-acid ratio during four stages of tomato fruit development. The presented data represent the average of three replicates, with error bars indicating the standard deviation. The same letter indicates no significant difference in mean values at p < 0.05 (Duncan’s test).
Figure 5. Contents of flavor-related compounds in tomato fruits. (A) Soluble solids content (SSC) during four stages of tomato fruit development. (B) Titratable acidity (TA) during four stages of tomato fruit development. (C) Sugar-to-acid ratio during four stages of tomato fruit development. The presented data represent the average of three replicates, with error bars indicating the standard deviation. The same letter indicates no significant difference in mean values at p < 0.05 (Duncan’s test).
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Figure 6. Levels of nutritional components in tomato fruits. (A) Soluble protein content in tomato fruits at four developmental stages. (B) Ascorbic acid (Vc) content in tomato fruits at four developmental stages. The data presented are the average values of three replicates, and the error bars represent the standard deviation. The same letter indicates no significant difference at p < 0.05 (Duncan’s test).
Figure 6. Levels of nutritional components in tomato fruits. (A) Soluble protein content in tomato fruits at four developmental stages. (B) Ascorbic acid (Vc) content in tomato fruits at four developmental stages. The data presented are the average values of three replicates, and the error bars represent the standard deviation. The same letter indicates no significant difference at p < 0.05 (Duncan’s test).
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He, Z.; Wen, C.; Xu, W. Effects of Endogenous Melatonin Deficiency on the Growth, Productivity, and Fruit Quality Properties of Tomato Plants. Horticulturae 2023, 9, 851. https://doi.org/10.3390/horticulturae9080851

AMA Style

He Z, Wen C, Xu W. Effects of Endogenous Melatonin Deficiency on the Growth, Productivity, and Fruit Quality Properties of Tomato Plants. Horticulturae. 2023; 9(8):851. https://doi.org/10.3390/horticulturae9080851

Chicago/Turabian Style

He, Zhuo, Cen Wen, and Wen Xu. 2023. "Effects of Endogenous Melatonin Deficiency on the Growth, Productivity, and Fruit Quality Properties of Tomato Plants" Horticulturae 9, no. 8: 851. https://doi.org/10.3390/horticulturae9080851

APA Style

He, Z., Wen, C., & Xu, W. (2023). Effects of Endogenous Melatonin Deficiency on the Growth, Productivity, and Fruit Quality Properties of Tomato Plants. Horticulturae, 9(8), 851. https://doi.org/10.3390/horticulturae9080851

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