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Review
. 2019 Jan 24;9:2006.
doi: 10.3389/fpls.2018.02006. eCollection 2018.

Vitamin C Content in Fruits: Biosynthesis and Regulation

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Free PMC article
Review

Vitamin C Content in Fruits: Biosynthesis and Regulation

Mario Fenech et al. Front Plant Sci. .
Free PMC article

Abstract

Throughout evolution, a number of animals including humans have lost the ability to synthesize ascorbic acid (ascorbate, vitamin C), an essential molecule in the physiology of animals and plants. In addition to its main role as an antioxidant and cofactor in redox reactions, recent reports have shown an important role of ascorbate in the activation of epigenetic mechanisms controlling cell differentiation, dysregulation of which can lead to the development of certain types of cancer. Although fruits and vegetables constitute the main source of ascorbate in the human diet, rising its content has not been a major breeding goal, despite the large inter- and intraspecific variation in ascorbate content in fruit crops. Nowadays, there is an increasing interest to boost ascorbate content, not only to improve fruit quality but also to generate crops with elevated stress tolerance. Several attempts to increase ascorbate in fruits have achieved fairly good results but, in some cases, detrimental effects in fruit development also occur, likely due to the interaction between the biosynthesis of ascorbate and components of the cell wall. Plants synthesize ascorbate de novo mainly through the Smirnoff-Wheeler pathway, the dominant pathway in photosynthetic tissues. Two intermediates of the Smirnoff-Wheeler pathway, GDP-D-mannose and GDP-L-galactose, are also precursors of the non-cellulosic components of the plant cell wall. Therefore, a better understanding of ascorbate biosynthesis and regulation is essential for generation of improved fruits without developmental side effects. This is likely to involve a yet unknown tight regulation enabling plant growth and development, without impairing the cell redox state modulated by ascorbate pool. In certain fruits and developmental conditions, an alternative pathway from D-galacturonate might be also relevant. We here review the regulation of ascorbate synthesis, its close connection with the cell wall, as well as different strategies to increase its content in plants, with a special focus on fruits.

Keywords: ascorbic acid; biosynthesis; cell wall; fruit; regulation; vitamin C.

Figures

FIGURE 1
FIGURE 1
Main fruit crops yield and consumption according to FAO. (A) Global fruit production, in million tons, and its evolution from 1961 to 2016. (B) Fruit ascorbate intake, in grams of ascorbate capita-1 year-1, in the countries from the European Union in 2013. Data were generated considering ascorbate (VitC) levels of raw fruit available in USDA database (https://ndb.nal.usda.gov/ndb/search/list) and consumption data of each fruit (Kg capita-1 year-1) from FAOSTAT. USDA IDs consulted: 9200 (Oranges includes mandarins, raw, all commercial varieties), 11529 (Tomatoes, red, ripe, raw, year average), 9003 (Apples, raw with skin), 9132 [Grapes, red or green (European type, such as Thompson seedless), raw], 9266 (Pineapple, raw, all varieties), 9040 (Bananas, raw). Consumption data was obtained from Eurostat (http://ec.europa.eu/eurostat). (C) Evolution in the global consumption of fruits, in Kg capita-1 year-1, from 1961 to 2013.
FIGURE 2
FIGURE 2
Biosynthesis pathways of ascorbate in the plant cell. Solid lines represent the committed reactions within a pathway. Dashed lines represent the translocation of a molecule from a cellular compartment to another. Enzymes are displayed in bold: PGI, phosphoglucose isomerase; PMI, phosphomannose isomerase; PMM, phosphomannomutase; GMP, GDP-D-mannose pyrophosphorylase (Arabidopsis VTC1); GME, GDP-D-mannose-3′,5′-isomerase; GGP, GDP-L-galactose phosphorylase (Arabidopsis VTC2/VTC5); GPP, L-galactose-1-phosphate phosphatase (Arabidopsis VTC4); L-GalDH, L-galactose dehydrogenase; GLDH, L-galactono-1,4-lactone dehydrogenase; cAPX, cytosolic Ascorbate Peroxidase; MDHAR, monodehydroascorbate reductase; DHAR, dehydroascorbate reductase; PHT4.4, inorganic phosphate transporter; sAPX, stromal ascorbate peroxidase; tAPX, thylakoidal ascorbate peroxidase; GMD, GDP-D-mannose-4,6-dehydratase (Arabidopsis MUR1/GMD1); GER, GDP-4-keto-6-deoxymannose-3,5-epimerase-4-reductase (Arabidopsis GER1/GER2); GalUR, D-Galacturonate Reductase. Substrates and products are shown in regular shape: Glc, glucose; Fru, fructose; Man, mannose; Gal, galactose; Gul, gulose; GalU, Galacturonate; Me-D-GalU, methyl galacturonate; GalA, Galactonate; GalL, L-galactono-1,4-lactone; Asc, ascorbate; CytCOX, oxidized cytochrome c; CytCRED, reduced cytochrome c; MDHA, monodehydroascorbate; DHA, dehydroascorbate; GDP-α-keto-6-dMan, GDP-4-keto-6-deoxymannose; Fuc, fucose; mOM, mitochondrial outer membrane; mIMS, mitochondrial inter membrane space; mIM, mitochondrial inner membrane; cOM, chloroplastic outer membrane; cIMS, chloroplastic inter membrane space; cIM, chloroplastic inner membrane.
FIGURE 3
FIGURE 3
GDP-D-mannose and its biological relevance for ascorbate and cell wall biosynthesis in plants. (A) Reaction scheme for the novo synthesis of GDP-D-mannose in Arabidopsis thaliana. Mutants described for each step are indicated in lower case italic red letters. (B) Biological impairment over cell wall (RG-II, rhamnogalacturonate II) and ascorbate content in mutants of genes controlling the GDP-D-mannose pool. MUR1 and GMD1 encode two GDP-D-mannose-4,6-dehydratases. GER1 and GER2 encode two GDP-4-keto-6-deoxymannose-3,5-epimerase-4-reductases. The epimerase reaction is reversible whereas the reduction is not (Bonin et al., 1997). VTC1 encodes GMP, a GDP-D-mannose pyrophosphorylase, GME encodes a GDP-D-mannose-3′,5′-isomerase. D-Man-1-P, D-mannose-1-phosphate; GDP-D-Man, GDP-D-mannose; GDP-L-Gul, GDP-D-gulose; GDP-D-Gal, GDP-D-galactose; GDP-D-Fuc, GDP-D-fucose; Asc, Ascorbate.

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References

    1. Agathocleous M., Meacham C. E., Burgess R. J., Piskounova E., Zhao Z., Crane G. M., et al. (2017). Ascorbate regulates haematopoietic stem cell function and leukaemogenesis. Nature 549 476–481. 10.1038/nature23876 - DOI - PMC - PubMed
    1. Agius F., González-Lamothe R., Caballero J. L., Muñoz-Blanco J., Botella M. A., Valpuesta V. (2003). Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase. Nat. Biotechnol. 21 177–181. 10.1038/nbt777 - DOI - PubMed
    1. Akhatou I., Fernández-Recamales Á. (2014). Nutritional and nutraceutical quality of strawberries in relation to harvest time and crop conditions. J. Agric. Food Chem. 62 5749–5760. 10.1021/jf500769x - DOI - PubMed
    1. Amaya I., Osorio S., Martinez-Ferri E., Lima-Silva V., Doblas V. G., Fernández-Muñoz R., et al. (2015). Increased antioxidant capacity in tomato by ectopic expression of the strawberry D – galacturonate reductase gene. Biotechnol. J. 10 490–500. 10.1002/biot.201400279 - DOI - PubMed
    1. Amaya I., Pillet J., Folta K. M. (2016). “Identification of genes responsible for natural variation in volatile content using next-generation sequencing technology,” in Plant Signal Transduction. Methods in Molecular Biology Vol. 1363 eds Botella J. R., Botella M. A., editors. (New York, NY: Humana Press; ),37–45. - PubMed

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