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      Vitamin C in Plants: From Functions to Biofortification

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          Abstract

          Vitamin C ( l-ascorbic acid) is an excellent free radical scavenger, not only for its capability to donate reducing equivalents but also for the relative stability of the derived monodehydroascorbate radical. However, vitamin C is not only an antioxidant, since it is also a cofactor for numerous enzymes involved in plant and human metabolism. In humans, vitamin C takes part in various physiological processes, such as iron absorption, collagen synthesis, immune stimulation, and epigenetic regulation. Due to the functional loss of the gene coding for l-gulonolactone oxidase, humans cannot synthesize vitamin C; thus, they principally utilize plant-based foods for their needs. For this reason, increasing the vitamin C content of crops could have helpful effects on human health. To achieve this objective, exhaustive knowledge of the metabolism and functions of vitamin C in plants is needed. In this review, the multiple roles of vitamin C in plant physiology as well as the regulation of its content, through biosynthetic or recycling pathways, are analyzed. Finally, attention is paid to the strategies that have been used to increase the content of vitamin C in crops, emphasizing not only the improvement of nutritional value of the crops but also the acquisition of plant stress resistance.

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          Most cited references204

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          The biosynthetic pathway of vitamin C in higher plants.

          Vitamin C (L-ascorbic acid) has important antioxidant and metabolic functions in both plants and animals, but humans, and a few other animal species, have lost the capacity to synthesize it. Plant-derived ascorbate is thus the major source of vitamin C in the human diet. Although the biosynthetic pathway of L-ascorbic acid in animals is well understood, the plant pathway has remained unknown-one of the few primary plant metabolic pathways for which this is the case. L-ascorbate is abundant in plants (found at concentrations of 1-5 mM in leaves and 25 mM in chloroplasts) and may have roles in photosynthesis and transmembrane electron transport. We found that D-mannose and L-galactose are efficient precursors for ascorbate synthesis and are interconverted by GDP-D-mannose-3,5-epimerase. We have identified an enzyme in pea and Arabidopsis thaliana, L-galactose dehydrogenase, that catalyses oxidation of L-galactose to L-galactono-1,4-lactone. We propose an ascorbate biosynthesis pathway involving GDP-D-mannose, GDP-L-galactose, L-galactose and L-galactono-1,4-lactone, and have synthesized ascorbate from GDP-D-mannose by way of these intermediates in vitro. The definition of this biosynthetic pathway should allow engineering of plants for increased ascorbate production, thus increasing their nutritional value and stress tolerance.
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            Catalytic metals, ascorbate and free radicals: combinations to avoid.

            Trace levels of transition metals can participate in the metal-catalyzed Haber-Weiss reaction (superoxide-driven Fenton reaction) as well as catalyze the oxidation of ascorbate. Generally ascorbate is thought of as an excellent reducing agent; it is able to serve as a donor antioxidant in free radical-mediated oxidation processes. However, as a reducing agent it is also able to reduce redox-active metals such as copper and iron, thereby increasing the pro-oxidant chemistry of these metals. Thus ascorbate can serve as both a pro-oxidant and an antioxidant. In general, at low ascorbate concentrations, ascorbate is prone to be a pro-oxidant, and at high concentrations, it will tend to be an antioxidant. Hence there is a crossover effect. We propose that the "position" of this crossover effect is a function of the catalytic metal concentration. In this presentation, we discuss: (1) the role of catalytic metals in free radical-mediated oxidations; (2) ascorbate as both a pro-oxidant and an antioxidant; (3) catalytic metal catalysis of ascorbate oxidation; (4) use of ascorbate to determine adventitious catalytic metal concentrations; (5) use of ascorbate radical as a marker of oxidative stress; and (6) use of ascorbate and iron as free radical pro-oxidants in photodynamic therapy of cancer.
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              Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase.

              L-Ascorbic acid (vitamin C) in fruits and vegetables is an essential component of human nutrition. Surprisingly, only limited information is available about the pathway(s) leading to its biosynthesis in plants. Here, we report the isolation and characterization of GalUR, a gene from strawberry that encodes an NADPH-dependent D-galacturonate reductase. We provide evidence that the biosynthesis of L-ascorbic acid in strawberry fruit occurs through D-galacturonic acid, a principal component of cell wall pectins. Expression of GalUR correlated with changing ascorbic acid content in strawberry fruit during ripening and with variations in ascorbic acid content in fruit of different species of the genus Fragaria. Reduced pectin solubilization in cell walls of transgenic strawberry fruit with decreased expression of an endogenous pectate lyase gene resulted in lower ascorbic acid content. Overexpression of GalUR in Arabidopsis thaliana enhanced vitamin C content two- to threefold, demonstrating the feasibility of engineering increased vitamin C levels in plants using this gene.
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                Author and article information

                Journal
                Antioxidants (Basel)
                Antioxidants (Basel)
                antioxidants
                Antioxidants
                MDPI
                2076-3921
                29 October 2019
                November 2019
                : 8
                : 11
                : 519
                Affiliations
                Department of Biology, University of Bari “Aldo Moro”, Via E. Orabona 4, 70125 Bari, Italy; costantino.paciolla@ 123456uniba.it (C.P.); stefania.fortunato@ 123456uniba.it (S.F.); nunzio.dipierro@ 123456uniba.it (N.D.); annalisa.paradiso@ 123456uniba.it (A.P.); silvana.deleonardis@ 123456uniba.it (S.D.L.); linda.mastropasqua@ 123456uniba.it (L.M.)
                Author notes
                [* ]Correspondence: mariaconcetta.depinto@ 123456uniba.it ; Tel.: +39-080-544-2156
                Author information
                https://orcid.org/0000-0002-2184-0231
                https://orcid.org/0000-0002-2937-1935
                Article
                antioxidants-08-00519
                10.3390/antiox8110519
                6912510
                31671820
                2054c6ba-aae1-4705-9d4e-81f1be313b42
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 02 October 2019
                : 26 October 2019
                Categories
                Review

                ascorbate,antioxidant,biofortification,light,plant growth,reactive oxygen species,vitamin c

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