Regulation of Vitamin C Accumulation for Improved Tomato Fruit Quality and Alleviation of Abiotic Stress

Abstract

Ascorbic acid (AsA) is an essential multifaceted phytonutrient for both the human diet and plant growth. Optimum levels of AsA accumulation combined with balanced redox homeostasis are required for normal plant development and defense response to adverse environmental stimuli. Notwithstanding its moderate AsA levels, tomatoes constitute a good source of vitamin C in the human diet. Therefore, the enhancement of AsA levels in tomato fruit attracts considerable attention, not only to improve its nutritional value but also to stimulate stress tolerance. Genetic regulation of AsA concentrations in plants can be achieved through the fine-tuning of biosynthetic, recycling, and transport mechanisms; it is also linked to changes in the whole fruit metabolism. Emerging evidence suggests that tomato synthesizes AsA mainly through the l-galactose pathway, but alternative pathways through d-galacturonate or myo-inositol, or seemingly unrelated transcription and regulatory factors, can be also relevant in certain developmental stages or in response to abiotic factors. Considering the recent advances in our understanding of AsA regulation in model and other non-model species, this review attempts to link the current consensus with novel technologies to provide a comprehensive strategy for AsA enhancement in tomatoes, without any detrimental effect on plant growth or fruit development.

Keywords: ascorbate; biofortification; environmental stimuli; ethylene; genetic modifications; plant stress; postharvest.

Figure 1

AsA metabolic pathways in tomato. The main biosynthetic pathway occurring via l-galactose is shown in brown, the d-galacturonate pathway in green, the d-glucuronate pathway in blue, and the AsA recycling pathway in black. Purple symbolizes a reaction taking place in the apoplast. Efficient manipulations of structural genes in either leaves (green) or fruits (red) via transgenic efforts are presented on the left of the reactions with blue arrows, followed by their impact on the AsA pool (increase, decrease, or stable). The fold change >1.5 (overexpression) or <0.5 (silencing) of the AsA contents in transgenic plants compared to wild-type plants was regarded as efficient manipulation. The full list of transgenic approaches is given in Table 1. Regulatory factors affecting positively or negatively the transcription of structural genes are also presented with arrows on the right of the reaction. PGI: Phosphoglucose Isomerase; PMI: Mannose-6-phosphate isomerase; PMM: Phosphomannomutase; GMP: GDP-d-mannose pyrophosphorylase; GME: GDP-d-mannose 3′5′ epimerase; GGP: GDP-l-galactose-phosphorylase; GPP: l-galactose-1-P phosphatase; GalDH: L-galactose dehydrogenase; GLDH: L-galactono-1,4-lactone dehydrogenase; GalUR: D-galacturonate reductase; MIOX: myo-inositol oxygenase; GuLO: L-gulono-1,4-lactone dehydrogenase; AO: ascorbate oxidase; APX: ascorbate peroxidase; MDHAR: monodehydro-ascorbate reductase; DHAR: dehydro-ascorbate reductase; MDHA: monodehydroascorbate; DHA: dehydroascorbate; GSH: glutathione; GSSG: oxidized glutathione.

Figure 2

Schematic diagram of postharvest abiotic stress of tomato fruit and oxidative stress response. Fruit exposure to postharvest abiotic stress conditions such as wounding, chilling temperature, CO₂/O₂ injury, and dehydration, provoke a significant increase in ethylene (C₂H₄) and reactive oxygen species (ROS), which in low concentration serve as signaling molecules to regulate biological and physiological processes, whereas in high concentration can cause important damage to molecules and cell structure. Fruits organize an elaborate antioxidant network system as a defense mechanism, with AsA playing an important role especially by the robust enhancement of the AsA-GSH pathway, accompanied by a slower response of AsA biosynthesis.