Exogenous methyl jasmonate regulates sucrose metabolism in tomato during postharvest ripening
Introduction
Fruit ripening is a complex process characterized by the accumulation of carbohydrates (Cherian et al., 2014), which provide energy for fruit development and contribute to its flavor (Li et al., 2012; Rolland et al., 2002; Zhu et al., 2013). Sugar, the carbon source of energy for plant growth, is converted to various metabolites in the fruit (Ai et al., 2016; Huang et al., 2016; Qin et al., 2016). Multiple studies have reported the accumulation of sugars during fruit ripening (Bianco and Rieger, 2002; Fait et al., 2008; Osorio et al., 2012). Tomato (Solanum lycopersicum), due to genome availability, dramatic metabolic changes, and short life cycle, is an excellent model to study fruit development and ripening (Bastias et al., 2011; Gapper et al., 2013; Klee and Tieman, 2013; Osorio et al., 2011). Various physiological, metabolic, and genetic processes comprehensively result in sugar accumulation in tomato (Baldet et al., 2006; Mounet et al., 2009), and the accumulation continues after harvest via the metabolism of stored carbohydrates, lipids, and proteins (Baldet et al., 2002; Patrick et al., 2013). The sensory quality of tomato fruit is closely associated with the balance between sugar and organic acid contents (Osorio et al., 2013; Roessner-Tunali et al., 2003). Wild green tomato contains higher sucrose levels than the red one, which primarily contains glucose and fructose with only little sucrose (Miron and Schaffer, 1991). During the last growth phase in tomato, metabolism changes drastically as the fruit ripens, while glucose and fructose continue to accumulate (Carrari et al., 2006).
Sucrose and its hydrolysis products (fructose and glucose) play an essential role in regulating fruit growth, development, and ripening (Koch, 2004; Qin et al., 2016; Ruan, 2014; Ruan et al., 2010; Tognetti et al., 2013). Sucrose metabolism is associated with three major enzymes, including sucrose phosphate synthase (SPS), sucrose synthase (SUS), and acid invertase (AI). Specifically, SPS, the key enzyme involved in the translocation of photoassimilates from source to sink, transfers the glucosyl moiety from UDP-glucose to fructose-6-phosphate, which is dephosphorylated by the action of sucrose-6-phosphate phosphatase (SPP) to finally yield sucrose (Patrick et al., 2013); SUS and AI convert sucrose into glucose and fructose (Geiger et al., 1996; Ruan et al., 2010). Furthermore, sucrose metabolism is associated with the corresponding genes SPS (Chen et al., 2005), AI (Ranwala et al., 1991), and SUS, which affect sucrose biosynthesis and degradation (Hou et al., 2014).
The volatile ester methyl jasmonate (MeJA) and other derivatives of jasmonic acid (JA), collectively known as JAs, exist naturally in a wide range of higher plants (Wasternack and Hause, 2013). They function as elicitors or signaling molecules that mediate plant responses to environmental stresses and regulate the developmental processes, including root growth, seed germination, pollen development, and fruit development (Rohwer and Erwin, 2008; Wasternack and Hause, 2013). Studies have shown that JAs play a vital role in fruit ripening both in climacteric and non-climacteric fruits (Concha et al., 2013; Kondo et al., 2007; Pena-Cortes et al., 2004; Rudell et al., 2002; Shu et al., 2020). Exogenous MeJA increased the sucrose content and enhanced the chilling tolerance of peach fruit during cold storage (Yu et al., 2016). However, knowledge of the role of MeJA in regulating sucrose metabolism during tomato ripening is still obscure. Therefore, this study investigates the effects of exogenous MeJA on the sugar contents, the enzymatic activities and gene expression levels related to sucrose metabolism in tomato during postharvest ripening. These findings will provide new insights into the regulation of sucrose metabolism by MeJA during tomato ripening.
Section snippets
Plant materials
Cherry tomato (Solanum lycopersicum cv. Xin Taiyang) fruit were harvested manually at the mature green stage from a greenhouse (20−25 °C, 70–85 % relative humidity) in Xiaoshan County (Zhejiang Province, China). Fruit of uniform shape and size with no injuries were chosen from about 150 tomato plants at the second inflorescence (about 0.5 m above the ground), and transported to the laboratory within two hours. Each fruit was disinfected in 0.3 % (v/v) sodium hypochlorite solution for 3 min,
Effects of MeJA on fruit color, firmness, and ethylene production
As shown in Fig. 1a, obvious morphological differences were observed between MeJA-treated and control fruit during tomato ripening. A significant acceleration in ripening was observed during 4–10 d after MeJA treatment. MeJA-treated fruit showed distinct color transition at 4 d, which was 3 d earlier than the control fruit (Fig. 1a). A higher a* value was observed in MeJA-treated fruit during 4–10 d than the control fruit (Fig. 1b). Meanwhile, the firmness of MeJA-treated fruit decreased
Discussion
Fruit ripening is a complex process that involves a series of physiological and biochemical changes, which ultimately influence the fruit quality characteristics, such as color, texture, aroma, and flavor (Seymour et al., 2013; Shen et al., 2014). In the present study, exogenous MeJA enhanced fruit color transition, firmness decrease, and ethylene production increase during tomato ripening, which was consistent with the earlier reports in tomato (Min et al., 2020; Saniewski et al., 1987), apple
Conclusions
In the present study, exogenous MeJA enhanced sucrose accumulation, whereas it inhibited fructose and glucose accumulation in tomato. High SPS activity and low AI and NI activities were observed along with the upregulation of genes associated with sucrose biosynthesis and the downregulation of genes associated with sucrose degradation during ripening in MeJA-treated fruit. The results suggest that MeJA may influence sucrose metabolism via regulating the transcript abundance of the related genes
Author contributions statement
Xiaoya Tao, Qiong Wu and Tiejin Ying conceived and designed the experiment; Xiaoya Tao performed the experiment, analyzed the data, prepared the figures and wrote the manuscript; Qiong Wu, Jiayin Li, Luyun Cai, Linchun Mao, Zisheng Luo, Li Li and Tiejin Ying modified the paper. All the authors have approved the final revised manuscript.
Declaration of Competing Interest
None.
Acknowledgements
The research was supported by the National Key Research and Development Program of China (2017YFD0401304) and Youth Program of National Natural Science Foundation of China (32001753).
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