Exogenous methyl jasmonate regulates sucrose metabolism in tomato during postharvest ripening

https://doi.org/10.1016/j.postharvbio.2021.111639Get rights and content

Highlights

  • Expediting effect of MeJA on ripening was evaluated in postharvest tomato.

  • MeJA accelerated sucrose accumulation by changing the activities of SPS, AI and NI.

  • MeJA inhibited the accumulation of fructose and glucose by altering the enzymes.

  • MeJA changed the expression levels of key genes involved in sucrose metabolism.

Abstract

Sucrose metabolism is a fundamental process during tomato ripening. Studies have shown the role of the phytohormone methyl jasmonate (MeJA) in tomato fruit ripening. However, the role of MeJA in regulating sucrose metabolism in tomato is still unclear. In this study, mature green cherry tomato fruit were infiltrated with MeJA (0.5 mM) or sterile deionized water (control). The changes in color, firmness, and ethylene production in fruit, the contents of sucrose, glucose and fructose, and the enzymatic activities and the expression levels of key genes associated with sucrose metabolism were determined periodically during a storage period of 16 d. MeJA-treated fruit showed a significant acceleration in ripening, with higher a* value and ethylene production and lower firmness. MeJA treatment enhanced sucrose phosphate synthase (SPS) activity, whereas it inhibited acid invertase (AI) and neutral invertase (NI) activities. These changes in enzyme activities together resulted in a significantly higher sucrose content and lower glucose and fructose contents. Furthermore, exogenous MeJA upregulated the gene expression levels of sucrose-phosphate synthase1–4 (SPS1-4) and sucrose-phosphate phosphatase2 (SPP2), which were associated with sucrose biosynthesis, and downregulated those related to sucrose degradation, except for sucrose synthase2 (SUS2) and SUS3. The findings indicated that exogenous MeJA might alter sucrose metabolism during tomato ripening by regulating the enzymatic activities and gene expression levels. This research provides valuable information to elucidate the mechanisms via which MeJA regulates tomato sucrose metabolism.

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).

References (100)

  • J.Y. Lv et al.

    Effects of methyl jasmonate on expression of genes involved in ethylene biosynthesis and signaling pathway during postharvest ripening of apple fruit

    Sci. Hortic-Amsterdam

    (2018)
  • M. Okamura et al.

    Tissue specificity and diurnal change in gene expression of the sucrose phosphate synthase gene family in rice

    Plant Sci.

    (2011)
  • Y.L. Ruan et al.

    Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat

    Mol. Plant

    (2010)
  • C. Salles et al.

    Determination and gustatory properties of taste-active compounds in tomato juice

    Food Chem.

    (2003)
  • M.E. Salvucci et al.

    Purification and photoaffinity-labeling of sucrose phosphate synthase from spinach leaves

    Arch. Biochem. Biophys.

    (1990)
  • W.E. Schafer et al.

    Partial purification and characterisation of sucrose synthase in sugarcane

    J. Plant Physiol.

    (2005)
  • K. Wang et al.

    The metabolism of soluble carbohydrates related to chilling injury in peach fruit exposed to cold stress

    Postharvest Biol. Tec.

    (2013)
  • N. Wang et al.

    Involvement of vacuolar processing enzyme SlVPE5 in post-transcriptional process of invertase in sucrose accumulation in tomato

    Plant Physiol. Biochem.

    (2016)
  • M.M. Yu et al.

    The effect of MeJA on ethylene biosynthesis and induced disease resistance to Botrytis cinerea in tomato

    Postharvest Biol. Tec.

    (2009)
  • M.M. Yu et al.

    Methyl jasmonate-induced defense responses are associated with elevation of 1-aminocyclopropane-1-carboxylate oxidase in Lycopersicon esculentum fruit

    J. Plant Physiol.

    (2011)
  • L.N. Yu et al.

    Effects of hot air and methyl jasmonate treatment on the metabolism of soluble sugars in peach fruit during cold storage

    Postharvest Biol. Tec.

    (2016)
  • L.N. Yu et al.

    Sucrose degradation is regulated by 1-methycyclopropene treatment and is related to chilling tolerance in two peach cultivars

    Postharvest Biol Tec

    (2017)
  • Z. Zhu et al.

    Characterisation of genes encoding key enzymes involved in sugar metabolism of apple fruit in controlled atmosphere storage

    Food Chem.

    (2013)
  • A. Albacete et al.

    Hormonal and metabolic regulation of tomato fruit sink activity and yield under salinity

    J. Exp. Bot.

    (2014)
  • P. Baldet et al.

    Contrasted responses to carbohydrate limitation in tomato fruit at two stages of development

    Plant Cell Environ.

    (2002)
  • P. Baldet et al.

    The expression of cell proliferation-related genes in early developing flowers is affected by a fruit load reduction in tomato plants

    J. Exp. Bot.

    (2006)
  • A. Bastias et al.

    Modulation of organic acids and sugar content in tomato fruits by an abscisic acid-regulated transcription factor

    Physiol. Plant.

    (2011)
  • R.L. Bianco et al.

    Partitioning of sorbitol and sucrose catabolism within peach fruit

    J. Am. Soc. Hortic. Sci.

    (2002)
  • Z. Bieniawska et al.

    Analysis of the sucrose synthase gene family in Arabidopsis

    Plant J.

    (2007)
  • F.C. Botha et al.

    Sucrose phosphate synthase and sucrose synthase activity during maturation of internodal tissue in sugarcane

    Aust. J. Plant Physiol.

    (2000)
  • F. Carrari et al.

    Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior

    Plant Physiol.

    (2006)
  • S. Chen et al.

    Differential expression of sucrose-phosphate synthase isoenzymes in tobacco reflects their functional specialization during dark-governed starch mobilization in source leaves

    Plant Physiol.

    (2005)
  • S. Cherian et al.

    ’MOvers and shakers’ in the regulation of fruit ripening: a cross-dissection of climacteric versus non-climacteric fruit

    J. Exp. Bot.

    (2014)
  • C. Davies et al.

    Sugar accumulation in grape berries - Cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissues

    Plant Physiol.

    (1996)
  • Q.D. Dinh et al.

    Exploring natural genetic variation in tomato sucrose synthases on the basis of increased kinetic properties

    PLoS One

    (2018)
  • J.R.O. do Nascimento et al.

    Sucrose synthase activity and expression during development and ripening in bananas

    J. Plant Physiol.

    (2000)
  • D.C. Doehlert et al.

    Enzymes of sucrose and hexose metabolism in developing kernels of two inbreds of maize

    Plant Physiol.

    (1988)
  • A. Fait et al.

    Reconfiguration of the achene and receptacle metabolic networks during strawberry fruit development

    Plant Physiol.

    (2008)
  • H. Fallahi et al.

    Localization of sucrose synthase in developing seed and siliques of Arabidopsis thaliana reveals diverse roles for SUS during development

    J. Exp. Bot.

    (2008)
  • E. Fridman et al.

    Zooming in on a quantitative trait for tomato yield using interspecific introgressions

    Science

    (2004)
  • H.Y. Fu et al.

    Sink-associated and vascular-associated sucrose synthase functions are encoded by different gene classes in potato

    Plant Cell

    (1995)
  • N.E. Gapper et al.

    Molecular and genetic regulation of fruit ripening

    Plant Mol. Biol.

    (2013)
  • D.R. Geiger et al.

    Effect of environmental factors on whole plant assimilate partitioning and associated gene expression

    J. Exp. Bot.

    (1996)
  • S. Goren et al.

    Comparison of a novel tomato sucrose synthase, SlSUS4, with previously described SlSUS isoforms reveals distinct sequence features and differential expression patterns in association with stem maturation

    Planta

    (2011)
  • S. Goren et al.

    Suppression of sucrose synthase affects auxin signaling and leaf morphology in tomato

    PLoS One

    (2017)
  • J.M. Guo et al.

    Carbon assimilation, partitioning and export in mature cladophylls of two asparagus (Asparagus officinalis) cultivars with contrasting yield

    Physiol. Plantarum

    (2002)
  • M. Hothorn et al.

    Structural insights into the target specificity of plant invertase and pectin methylesterase inhibitory proteins

    Plant Cell

    (2004)
  • J. Hou et al.

    Global selection on sucrose synthase haplotypes during a century of wheat breeding

    Plant Physiol.

    (2014)
  • H. Huang et al.

    Sucrose and ABA regulate starch biosynthesis in maize through a novel transcription factor, ZmEREB156

    Sci. Rep. UK

    (2016)
  • M.S. Islam

    Sucrose metabolism in domesticated cherry tomato, Lycopersicon esculentum var. Cerasiforme Alef., and purification of sucrose synthase

    J. Hortic Sci. Biotech.

    (2001)
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