Abstract
BackgroundTomato is an economically important crop with fruits that are a significant source of bioactive compounds such as ascorbic acid and phenolics. Nowadays, the majority of the enzymes of the biosynthetic pathways and of the structural genes controlling the production and the accumulation of antioxidants in plants are known; however, the mechanisms that regulate the expression of these genes are yet to be investigated. Here, we analyzed the transcriptomic changes occurring during ripening in the fruits of two tomato cultivars (E1 and E115), characterized by a different accumulation of antioxidants, in order to identify candidate genes potentially involved in the biosynthesis of ascorbic acid and phenylpropanoids.ResultsRNA sequencing analyses allowed identifying several structural and regulator genes putatively involved in ascorbate and phenylpropanoids biosynthesis in tomato fruits. Furthermore, transcription factors that may control antioxidants biosynthesis were identified through a weighted gene co-expression network analysis (WGCNA). Results obtained by RNA-seq and WGCNA analyses were further confirmed by RT-qPCR carried out at different ripening stages on ten cultivated tomato genotypes that accumulate different amount of bioactive compounds in the fruit. These analyses allowed us to identify one pectin methylesterase, which may affect the release of pectin-derived D-Galacturonic acid as metabolic precursor of ascorbate biosynthesis. Results reported in the present work allowed also identifying one L-ascorbate oxidase, which may favor the accumulation of reduced ascorbate in tomato fruits. Finally, the pivotal role of the enzymes chalcone synthases (CHS) in controlling the accumulation of phenolic compounds in cultivated tomato genotypes and the transcriptional control of the CHS genes exerted by Myb12 were confirmed.ConclusionsBy using transcriptomic analyses, candidate genes encoding transcription factors and structural genes were identified that may be involved in the accumulation of ascorbic acid and phenylpropanoids in tomato fruits of cultivated genotypes. These analyses provided novel insights into the molecular mechanisms controlling antioxidants accumulation in ripening tomato fruits. The structural genes and regulators here identified could also be used as efficient genetic markers for selecting high antioxidants tomato cultivars.
Highlights
Tomato is an economically important crop with fruits that are a significant source of bioactive compounds such as ascorbic acid and phenolics
The two tomato genotypes were grown in open field and phenotypic and transcriptomic analyses of fruits were performed at three developmental stages: mature green (MG), breaker (BR) and mature red (MR)
Among the structural genes of the ascorbic acid pathways (Fig. 2), we identified one gene involved in the GDP-L-fucose biosynthesis (Solyc02g084210), coding for a GDP-mannose-4,6-dehydratase, which was up-regulated in E115 vs E1 in the BR and MR stages and that could be involved in alternatives Ascorbic acid (AsA) biosynthetic pathways
Summary
Tomato is an economically important crop with fruits that are a significant source of bioactive compounds such as ascorbic acid and phenolics. Consumption of tomato fruits, fresh or processed, is associated with a reduced risk of cancer, inflammation and chronic non-communicable diseases (CNCD) including cardiovascular diseases (CVD) [1, 2]. These health effects are due to the presence in tomato fruits of bioactive substances such as vitamin C (ascorbic acid), polyphenols and carotenoids [3]. Ascorbic acid (AsA), which cannot be synthesized by human body, shows significant ability as electron donor and potent antioxidant in human; it exerts a relevant role in protecting DNA from oxidant species induced damages and in the prevention of inflammation; it protects against oxidation of LDL (low-density lipoprotein) by different types of oxidative stress [4, 5]. Ascorbate can scavenge reactive oxygen species produced by photosynthesis and plays an important role in cell expansion, cell division, developmental processes and responses to stresses [8]
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