L-Ascorbic acid (vitamin C) is as essential to plants as it is to animals. Ascorbic acid functions as a major redox buffer and as a cofactor for enzymes involved in regulating photosynthesis, hormone biosynthesis, and regenerating other antioxidants. Ascorbic acid regulates cell division and growth and is involved in signal transduction. In contrast to the single pathway responsible for ascorbic acid biosynthesis in animals, plants use multiple pathways to synthesize ascorbic acid, perhaps reflecting the importance of this molecule to plant health. Given the importance of ascorbic acid to human nutrition, several technologies have been developed to increase the ascorbic acid content of plants through the manipulation of biosynthetic or recycling pathways. This paper provides an overview of these approaches as well as the consequences that changes in ascorbic acid content have on plant growth and function. Discussed is the capacity of plants to tolerate changes in ascorbic acid content. The many functions that ascorbic acid serves in plants, however, will require highly targeted approaches to improve their nutritional quality without compromising their health. 1. Introduction Vitamin C (L-ascorbic acid) is a water-soluble antioxidant that serves a predominantly protective role. Despite the fact that most mammals can synthesize ascorbate (Asc), humans (along with other primates, bats, and guinea pigs) are unable to make vitamin C as a result of a mutation to the gene encoding L-gulono-1,4-lactone oxidase, the last enzyme in the Asc biosynthetic pathway [1]. Although the symptoms associated with severe vitamin C deficiency, for example, weak joints, bleeding gums, and skin discoloration due to ruptured blood vessels, had been observed and described as early as 1497 by Vasco da Gama among his crew during their voyage around the southern tip of Africa to India, it was not until 1747 that James Lind demonstrated that consumption of citrus fruit prevented or cured the disorders associated with scurvy. Because of this, vitamin C was originally referred to as the “antiscorbutic factor.” Vitamin C (L-threo-hex-2-enono-1,4-lactone) was eventually isolated in 1928 by Dr. Szent-Gyorgyi although he was uncertain of its function. Only in 1932 did crystallization of the physiologically active compound isolated from natural sources identify the antiscorbutic factor as vitamin C [2–4], and its structure determined the following year [5]. In animals, ascorbate is involved in the synthesis of carnitine and collagen, an important component of skin, scar tissue, tendons,
References
[1]
I. B. Chatterjee, “Evolution and the biosynthesis of ascorbic acid,” Science, vol. 182, no. 4118, pp. 1271–1272, 1973.
[2]
J. L. Svirbely and A. Szent-Gy？rgyi, “Hexuronic acid as the antiscorbutic factor,” Nature, vol. 129, no. 3259, p. 576, 1932.
[3]
J. Tillmans and P. Hirsch, “Vitamin C,” Biochem Z, vol. 250, pp. 312–320, 1932.
[4]
W. A. Waugh and C. G. King, “The isolation and identification of vitamin C,” The Journal of Biological Chemistry, vol. 97, pp. 325–331, 1932.
[5]
R. W. Herbert, E. L. Hirst, E. G. V. Percival, R. J. W. Reynolds, and F. Smith, “The constitution of ascorbic acid,” Journal of the Chemical Society, pp. 1270–1290, 1933.
[6]
M. Levine, “New concepts in the biology and biochemistry of ascorbic acid,” The New England Journal of Medicine, vol. 314, no. 14, pp. 892–902, 1986.
[7]
M. Levine, C. C. Cantilena, and K. R. Dhariwal, “Determination of optimal vitamin C requirements in humans,” The American Journal of Clinical Nutrition, vol. 62, pp. 1347S–1356S., 1995.
[8]
H. Sies and W. Stahl, “Vitamins E and C, β-carotene, and other carotenoids as antioxidants,” American Journal of Clinical Nutrition, vol. 62, no. 6, pp. 1315S–1321S, 1995.
[9]
Food and Nutrition Board and Institute of Medicine, Vitamin C. Dietary Reference Intakes for Vitamin C, Vitamin E, Selenium, and Carotenoids, National Academy Press, Washington DC, USA, 2000.
[10]
C. S. Johnston and L. L. Thompson, “Vitamin C status of an outpatient population,” Journal of the American College of Nutrition, vol. 17, no. 4, pp. 366–370, 1998.
[11]
Z. Chen, T. E. Young, J. Ling, S. C. Chang, and D. R. Gallie, “Increasing vitamin C content of plants through enhanced ascorbate recycling,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 6, pp. 3525–3530, 2003.
[12]
R. D. Hancock and R. Viola, “Improving the nutritional value of crops through enhancement of L-ascorbic acid (vitamin C) content: rationale and biotechnological opportunities,” Journal of Agricultural and Food Chemistry, vol. 53, no. 13, pp. 5248–5257, 2005.
[13]
S. Naqvi, C. Zhu, G. Farre et al., “Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 19, pp. 7762–7767, 2009.
[14]
C. Pignocchi and C. H. Foyer, “Apoplastic ascorbate metabolism and its role in the regulation of cell signalling,” Current Opinion in Plant Biology, vol. 6, no. 4, pp. 379–389, 2003.
[15]
N. Smirnoff and G. L. Wheeler, “Ascorbic acid in plants: biosynthesis and function,” Critical Reviews in Plant Sciences, vol. 19, no. 4, pp. 267–290, 2000.
[16]
N. Smirnoff and G. L. Wheeler, “Ascorbic acid in plants: biosynthesis and function,” Critical Reviews in Biochemistry and Molecular Biology, vol. 35, no. 4, pp. 291–314, 2000.
[17]
N. M. Kerk and L. J. Feldman, “A biochemical model for the initiation and maintenance of the quiescent center: Implications for organization of root meristems,” Development, vol. 121, no. 9, pp. 2825–2833, 1995.
[18]
G. Noctor, S. Veljovic-Jovanovic, C. H. Foyer, and S. Grace, “Peroxide processing in photosynthesis: antioxidant coupling and redox signalling,” Philosophical Transactions of the Royal Society B, vol. 355, no. 1402, pp. 1465–1475, 2000.
[19]
J. J. Burns, “Ascorbic acid,” in Metabolic Pathways, D. M. Greenberg, Ed., vol. 1, pp. 394–411, Academic Press, New York, NY, USA, 3rd edition, 1967.
[20]
G. L. Wheeler, M. A. Jones, and N. Smirnoff, “The biosynthetic pathway of vitamin C in higher plants,” Nature, vol. 393, no. 6683, pp. 365–369, 1998.
[21]
B. A. Wolucka, G. Persiau, J. Van Doorsselaere et al., “Partial purification and identification of GDP-mannose , -epimerase of Arabidopsis thaliana, a key enzyme of the plant vitamin C pathway,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 26, pp. 14843–14848, 2001.
[22]
C. G. Bartoli, G. M. Pastori, and C. H. Foyer, “Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV,” Plant Physiology, vol. 123, no. 1, pp. 335–343, 2000.
[23]
E. Siendones, J. A. González-Reyes, C. Santos-Oca？a, P. Navas, and F. Córdoba, “Biosynthesis of ascorbic acid in kidney bean. L-Galactono-γ-lactone dehydrogenase is an intrinsic protein located at the mitochondrial inner membrane,” Plant Physiology, vol. 120, no. 3, pp. 907–912, 1999.
[24]
P. L. Conklin, J. E. Pallanca, R. L. Last, and N. Smirnoff, “L-Ascorbic acid metabolism in the ascorbate-deficient Arabidopsis mutant vtc1,” Plant Physiology, vol. 115, no. 3, pp. 1277–1285, 1997.
[25]
P. L. Conklin, E. H. Williams, and R. L. Last, “Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 18, pp. 9970–9974, 1996.
[26]
P. L. Conklin, S. Gatzek, G. L. Wheeler et al., “Arabidopsis thalianaVTC4 encodes L-galactose-1-P phosphatase, a plant ascorbic acid biosynthetic enzyme,” Journal of Biological Chemistry, vol. 281, no. 23, pp. 15662–15670, 2006.
[27]
P. L. Conklin, S. R. Norris, G. L. Wheeler, E. H. Williams, N. Smirnoff, and R. L. Last, “Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 7, pp. 4198–4203, 1999.
[28]
J. Dowdle, T. Ishikawa, S. Gatzek, S. Rolinski, and N. Smirnoff, “Two genes in Arabidopsis thaliana encoding GDP-L-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability,” Plant Journal, vol. 53, no. 3, p. 595, 2008.
[29]
W. A. Laing, M. A. Wright, J. Cooney, and S. M. Bulley, “The missing step of the L-galactose pathway of ascorbate biosynthesis in plants, an L-galactose guanyltransferase, increases leaf ascorbate content,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 22, pp. 9534–9539, 2007.
[30]
C. L. Linster, T. A. Gomez, K. C. Christensen et al., “Arabidopsis VTC2 encodes a GDP-L-galactose phosphorylase, the last unknown enzyme in the Smirnoff-Wheeler pathway to ascorbic acid in plants,” Journal of Biological Chemistry, vol. 282, no. 26, pp. 18879–18885, 2007.
[31]
F. A. Loewus and S. Kelly, “The metabolism of D-galacturonic acid and its methyl ester in the detached ripening strawberry,” Archives of Biochemistry and Biophysics, vol. 95, no. 3, pp. 483–493, 1961.
[32]
V. Valpuesta and M. A. Botella, “Biosynthesis of L-ascorbic acid in plants: new pathways for an old antioxidant,” Trends in Plant Science, vol. 9, no. 12, pp. 573–577, 2004.
[33]
M. W. Davey, C. Gilot, G. Persiau et al., “Ascorbate biosynthesis in Arabidopsis cell suspension culture,” Plant Physiology, vol. 121, no. 2, pp. 535–543, 1999.
[34]
F. A. Isherwood, Y. T. Chen, and L. W. Mapson, “Synthesis of L-ascorbic acid in plants and animals,” The Biochemical Journal, vol. 56, no. 1, pp. 1–15, 1954.
[35]
F. Agius, R. González-Lamothe, J. L. Caballero, J. Mu？oz-Blanco, M. A. Botella, and V. Valpuesta, “Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase,” Nature Biotechnology, vol. 21, no. 2, pp. 177–181, 2003.
[36]
F. A. Loewus, “Tracer studies on ascorbic acid formation in plants,” Phytochemistry, vol. 2, no. 2, pp. 109–128, 1963.
[37]
S. Gatzek, G. L. Wheeler, and N. Smirnoff, “Antisense suppression of L-galactose dehydrogenase in Arabidopsis thaliana provides evidence for its role in ascorbate synthesis and reveals light modulated L-galactose synthesis,” Plant Journal, vol. 30, no. 5, pp. 541–553, 2002.
[38]
A. K. Jain and C. L. Nessler, “Metabolic engineering of an alternative pathway for ascorbic acid biosynthesis in plants,” Molecular Breeding, vol. 6, no. 1, pp. 73–78, 2000.
[39]
A. Lorence, B. I. Chevone, P. Mendes, and C. L. Nessler, “myo-Inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis,” Plant Physiology, vol. 134, no. 3, pp. 1200–1205, 2004.
[40]
B. A. Wolucka and M. Van Montagu, “GDP-mannose 3′,5′-epimerase forms GDP-L-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants,” Journal of Biological Chemistry, vol. 278, no. 48, pp. 47483–47490, 2003.
[41]
C. Wagner, M. Sefkow, and J. Kopka, “Construction and application of a mass spectral and retention time index database generated from plant GC/EI-TOF-MS metabolite profiles,” Phytochemistry, vol. 62, no. 6, pp. 887–900, 2003.
[42]
J. A. Radzio, A. Lorence, B. I. Chevone, and C. L. Nessler, “L-Gulono-1,4-lactone oxidase expression rescues vitamin C-deficient Arabidopsis (vtc) mutants,” Plant Molecular Biology, vol. 53, no. 6, pp. 837–844, 2003.
[43]
P. Askerlund and C. Larsson, “Transmembrane electron transport in plasma membrane vesicles loaded with an NADH-generating system or ascorbate,” Plant Physiology, vol. 96, no. 4, pp. 1178–1184, 1991.
[44]
N. Horemans, C. H. Foyer, and H. Asard, “Transport and action of ascorbate at the plant plasma membrane,” Trends in Plant Science, vol. 5, no. 6, pp. 263–267, 2000.
[45]
N. Horemans, C. H. Foyer, G. Potters, and H. Asard, “Ascorbate function and associated transport systems in plants,” Plant Physiology and Biochemistry, vol. 38, no. 7-8, pp. 531–540, 2000.
[46]
H. Goldenberg and E. Schweinzer, “Transport of vitamin C in animal and human cells,” Journal of Bioenergetics and Biomembranes, vol. 26, no. 4, pp. 359–367, 1994.
[47]
R. C. Rose, “Transport of ascorbic acid and other water-soluble vitamins,” Biochimica et Biophysica Acta, vol. 947, no. 2, pp. 335–366, 1988.
[48]
J. C. Vera, C. I. Rivas, J. Fischbarg, and D. W. Golde, “Mammalian facilitative hexose transporters mediate the transport of dehydroascorbic acid,” Nature, vol. 364, no. 6432, pp. 79–82, 1993.
[49]
U. Heber, N. G. Bukhov, C. Wiese, and R. Hedrich, “Energized uptake of ascorbate and dehydroascorbate from the apoplast of intact leaves in relation to apoplastic steady state concentrations of ascorbate,” Plant Biology, vol. 5, no. 2, pp. 151–158, 2003.
[50]
N. Horemans, H. Asard, and R. J. Caubergs, “Transport of ascorbate into plasma membrane vesicles of Phaseolus vulgaris L,” Protoplasma, vol. 194, no. 3-4, pp. 177–185, 1996.
[51]
N. Horemans, M. Asard, and R. J. Caubergs, “The ascorbate carrier of higher plant plasma membranes preferentially translocates the fully oxidized (dehydroascorbate) molecule,” Plant Physiology, vol. 114, no. 4, pp. 1247–1253, 1997.
[52]
N. Horemans, H. Asard, P. Van Gestelen, and R. J. Caubergs, “Facilitated diffusion drives transport of oxidised ascorbate molecules into purified plasma membrane vesicles of Phaseolus vulgaris,” Physiologia Plantarum, vol. 104, no. 4, pp. 783–789, 1998.
[53]
N. Horemans, G. Potters, R. J. Caubergs, and H. Asard, “Transport of ascorbate into protoplasts of Nicotiana tabacum Bright Yellow-2 cell line,” Protoplasma, vol. 205, no. 1–4, pp. 114–121, 1998.
[54]
A. A. F. Rautenkranz, Li Liantje, F. Machler, E. Martinoia, and J. J. Oertli, “Transport of ascorbic and dehydroascorbic acids across protoplast and vacuole membranes isolated from barley (Hordeum vulgare L. cv Gerbel) leaves,” Plant Physiology, vol. 106, no. 1, pp. 187–193, 1994.
[55]
V. G. Maurino, E. Grube, J. Zielinski, A. Schild, K. Fischer, and U. I. Flügge, “Identification and expression analysis of twelve members of the nucleobase-ascorbate transporter (NAT) gene family in Arabidopsis thaliana,” Plant and Cell Physiology, vol. 47, no. 10, pp. 1381–1393, 2006.
[56]
E. Beck, A. Burkert, and M. Hofmann, “Uptake of L-ascorbate by intact spinach chloroplasts,” Plant Physiology, vol. 73, pp. 41–45, 1983.
[57]
C. H. Foyer and M. Lelandais, “A comparison of the relative rates of transport of ascorbate and glucose across the thylakoid, chloroplast and plasmalemma membranes of pea leaf mesophyll cells,” Journal of Plant Physiology, vol. 148, no. 3-4, pp. 391–398, 1996.
[58]
A. Szarka, N. Horemans, G. Bánhegyi, and H. Asard, “Facilitated glucose and dehydroascorbate transport in plant mitochondria,” Archives of Biochemistry and Biophysics, vol. 428, no. 1, pp. 73–80, 2004.
[59]
V. R. Franceschi and N. M. Tarlyn, “L-Ascorbic acid is accumulated in source leaf phloem and transported to sink tissues in plants,” Plant Physiology, vol. 130, no. 2, pp. 649–656, 2002.
[60]
L. Tedone, R. D. Hancock, S. Alberino, S. Haupt, and R. Viola, “Long-distance transport of L-ascorbic acid in potato,” BMC Plant Biology, vol. 4, article 16, 2004.
[61]
R. D. Hancock, D. McRae, S. Haupt, and R. Viola, “Synthesis of L-ascorbic acid in the phloem,” BMC Plant Biology, vol. 3, article 7, 2003.
[62]
A. A. Badejo, K. Wada, Y. Gao et al., “Translocation and the alternative D-galacturonate pathway contribute to increasing the ascorbate level in ripening tomato fruits together with the D-mannose/L-galactose pathway,” Journal of Experimental Botany, vol. 63, pp. 229–239, 2012.
[63]
M. Eskling, P. O. Arvidsson, and H. E. ？kerlund, “The xanthophyll cycle, its regulation and components,” Physiologia Plantarum, vol. 100, no. 4, pp. 806–816, 1997.
[64]
K. Asada, “Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress photoinhibition of photosynthesis: from molecular mechanisms to the field,” in BIOS Scientific Publishers, N. R. Baker and J. R. Bowyer, Eds., pp. 129–142, Oxford, UK, 1994.
[65]
K. I. Kivirikko and T. Pihlajaniemi, “Collagen hydroxylases and the protein disulfide isomerase subunit of prolyl 4-hydroxylases,” Advances in Enzymology and Related Areas of Molecular Biology, vol. 72, pp. 325–398, 1998.
[66]
P. Wojtaszek, C. G. Smith, and G. P. Bolwell, “Ultrastructural localisation and further biochemical characterisation of prolyl 4-hydroxylase from Phaseolus vulgaris: comparative analysis,” International Journal of Biochemistry and Cell Biology, vol. 31, no. 3-4, pp. 463–477, 1999.
[67]
M. B. Davies, J. Austin, and D. A. Partridge, Vitamin C: Its Chemistry and Biochemistry, Royal Society of Chemistry, Cambridge, UK, 1991.
[68]
J. J. Smith, P. Ververidis, and P. John, “Characterization of the ethylene-forming enzyme partially purified from melon,” Phytochemistry, vol. 31, no. 5, pp. 1485–1494, 1992.
[69]
X. Qin and J. A. D. Zeevaart, “The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 26, pp. 15354–15361, 1999.
[70]
O. Arrigoni and M. C. De Tullio, “The role of ascorbic acid in cell metabolism: between gene-directed functions and unpredictable chemical reactions,” Journal of Plant Physiology, vol. 157, no. 5, pp. 481–488, 2000.
[71]
O. Arrigoni and M. C. De Tullio, “Ascorbic acid: much more than just an antioxidant,” Biochimica et Biophysica Acta, vol. 1569, no. 1–3, pp. 1–9, 2002.
[72]
P. Hedden and Y. Kamiya, “Gibberellin biosynthesis: enzymes, genes and their regulation,” Annual Review of Plant Biology, vol. 48, pp. 431–460, 1997.
[73]
T. Lange, “Purification and partial amino-acid sequence of gibberellin 20-oxidase from Cucurbita maxima L. endosperm,” Planta, vol. 195, no. 1, pp. 108–115, 1994.
[74]
L. Britsch, “Purification and characterization of flavone synthase I, a 2-oxoglutarate-dependent desaturase,” Archives of Biochemistry and Biophysics, vol. 282, no. 1, pp. 152–160, 1990.
[75]
L. Britsch, J. Dedio, H. Saedler, and G. Forkmann, “Molecular characterization of flavanone 3β-hydroxylases. Consensus sequence, comparison with related enzymes and the role of conserved histidine residues,” European Journal of Biochemistry, vol. 217, no. 2, pp. 745–754, 1993.
[76]
T. A. Holton, F. Brugliera, and Y. Tanaka, “Cloning and expression of flavonol synthase from Petunia hybrida,” Plant Journal, vol. 4, no. 6, pp. 1003–1010, 1993.
[77]
N. Smirnoff, “The function and metabolism of ascorbic acid in plants,” Annals of Botany, vol. 78, no. 6, pp. 661–669, 1996.
[78]
N. Smirnoff and C. Critchley, “Ascorbate biosynthesis and function in photoprotection,” Philosophical Transactions of the Royal Society B, vol. 355, no. 1402, pp. 1455–1464, 2000.
[79]
N. Smirnoff, “Ascorbic acid: metabolism and functions of a multi-facetted molecule,” Current Opinion in Plant Biology, vol. 3, no. 3, pp. 229–235, 2000.
[80]
C. Foyer, J. Rowell, and D. Walker, “Measurement of the ascorbate content of spinach leaf protoplasts and chloroplasts during illumination,” Planta, vol. 157, no. 3, pp. 239–244, 1983.
[81]
K. Asada and M. Takahashi, “Production and scavenging of active oxygen in photosynthesis,” in Photoinhibition, D. J. Kyle, C. B. Osmond, and C. J. Arntzen, Eds., pp. 227–287, Elsevier, Amsterdam, The Netherlands, 1987.
[82]
C. H. Foyer, “Oxygen metabolism and electron transport in photosynthesis,” in Oxidative Stress and the Molecular Biology of Antioxidant Defenses, J. G. Scandalios, Ed., pp. 587–621, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, NY, USA, 1997.
[83]
B. Halliwell and J. M. C. Gutteridge, Free Radicals in Biology and Medicine, Oxford University Press, New York, NY, USA, 2000.
[84]
R. Mittler, “Oxidative stress, antioxidants and stress tolerance,” Trends in Plant Science, vol. 7, no. 9, pp. 405–410, 2002.
[85]
J. Mano, é. Hideg, and K. Asada, “Ascorbate in thylakoid lumen functions as an alternative electron donor to photosystem II and photosystem I,” Archives of Biochemistry and Biophysics, vol. 429, no. 1, pp. 71–80, 2004.
[86]
J. Mano, T. Ushimaru, and K. Asada, “Ascorbate in thylakoid lumen as an endogenous electron donor to Photosystem II: protection of thylakoids from photoinhibition and regeneration of ascorbate in stroma by dehydroascorbate reductase,” Photosynthesis Research, vol. 53, no. 2-3, pp. 197–204, 1997.
[87]
G. Forti and A. M. Ehrenheim, “The role of ascorbic acid in photosynthetic electron transport,” Biochimica et Biophysica Acta, vol. 1183, no. 2, pp. 408–412, 1993.
[88]
S. Grace, R. Pace, and T. Wydrzynski, “Formation and decay of monodehydroascorbate radicals in illuminated thylakoids as determined by EPR spectroscopy,” Biochimica et Biophysica Acta, vol. 1229, no. 2, pp. 155–165, 1995.
[89]
K. Asada, “The water-water cycle as alternative photon and electron sinks,” Philosophical Transactions of the Royal Society B, vol. 355, pp. 1419–1431, 2000.
[90]
Y. Nakano and K. Asada, “Spinach chloroplasts scavenge hydrogen peroxide on illumination,” Plant and Cell Physiology, vol. 21, no. 7, pp. 1295–1307, 1980.
[91]
K. Asada, “The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons,” Annual Review of Plant Biology, vol. 50, pp. 601–639, 1999.
[92]
J. B. Mudd, “Biochemical basis for the toxicity of ozone,” in Plant Response to Air Pollution, M. Yunus and M. Iqba, Eds., pp. 267–284, Wiley & Sons, New York, NY, USA, 1997.
[93]
M. Schraudner, W. Moeder, C. Wiese et al., “Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3,” Plant Journal, vol. 16, no. 2, pp. 235–245, 1998.
[94]
Z. M. Pel, Y. Murata, G. Benning et al., “Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells,” Nature, vol. 406, no. 6797, pp. 731–734, 2000.
[95]
X. Zhang, L. Zhang, F. Dong, J. Gao, D. W. Galbraith, and C. P. Song, “Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba,” Plant Physiology, vol. 126, no. 4, pp. 1438–1448, 2001.
[96]
J. R. Koch, R. A. Creelman, S. M. Eshita, M. Seskar, J. E. Mullet, and K. R. Davis, “Ozone sensitivity in hybrid poplar correlates with insensitivity to both salicylic acid and jasmonic acid. The role of programmed cell death in lesion formation,” Plant Physiology, vol. 123, no. 2, pp. 487–496, 2000.
[97]
S. Pasqualini, C. Piccioni, L. Reale, L. Ederli, G. D. Della Torre, and F. Ferranti, “Ozone-induced cell death in tobacco cultivar Bel W3 plants. The role of programmed cell death in lesion formation,” Plant Physiology, vol. 133, no. 3, pp. 1122–1134, 2003.
[98]
M. V. Rao, J. R. Koch, and K. R. Davis, “Ozone: a tool for probing programmed cell death in plants,” Plant Molecular Biology, vol. 44, no. 3, pp. 345–358, 2000.
[99]
E. M. Aro, I. Virgin, and B. Andersson, “Photoinhibition of photosystem. II. Inactivation, protein damage and turnover,” Biochimica et Biophysica Acta, vol. 1143, no. 2, pp. 113–134, 1993.
[100]
Y. Nishiyama, S. I. Allakhverdiev, and N. Murata, “A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II,” Biochimica et Biophysica Acta, vol. 1757, no. 7, pp. 742–749, 2006.
[101]
P. L. Conklin, S. A. Saracco, S. R. Norris, and R. L. Last, “Identification of ascorbic acid-deficient Arabidopsis thaliana mutants,” Genetics, vol. 154, no. 2, pp. 847–856, 2000.
[102]
S. D. Veljovic-Jovanovic, C. Pignocchi, G. Noctor, and C. H. Foyer, “Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system,” Plant Physiology, vol. 127, no. 2, pp. 426–435, 2001.
[103]
P. Müller-Moulé, T. Golan, and K. K. Niyogi, “Ascorbate-deficient mutants of Arabidopsis grow in high light despite chronic photooxidative stress,” Plant Physiology, vol. 134, no. 3, pp. 1163–1172, 2004.
[104]
P. Müller-Moulé, P. L. Conklin, and K. K. Niyogi, “Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo,” Plant Physiology, vol. 128, no. 3, pp. 970–977, 2002.
[105]
P. Müller-Moulé, M. Havaux, and K. K. Niyogi, “Zeaxanthin deficiency enhances the high light sensitivity of an ascorbate-deficient mutant of Arabidopsis,” Plant Physiology, vol. 133, no. 2, pp. 748–760, 2003.
[106]
C. H. Foyer, H. Lopez-Delgado, J. F. Dat, and I. M. Scott, “Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling,” Physiologia Plantarum, vol. 100, no. 2, pp. 241–254, 1997.
[107]
C. Huang, W. He, J. Guo, X. Chang, P. Su, and L. Zhang, “Increased sensitivity to salt stress in an ascorbate-deficient Arabidopsis mutant,” Journal of Experimental Botany, vol. 56, no. 422, pp. 3041–3049, 2005.
[108]
O. Chew, J. Whelan, and A. H. Millar, “Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants,” Journal of Biological Chemistry, vol. 278, no. 47, pp. 46869–46877, 2003.
[109]
A. A. Grantz, D. A. Brummell, and A. B. Bennett, “Ascorbate free radical reductase mRNA levels are induced by wounding,” Plant Physiology, vol. 108, no. 1, pp. 411–418, 1995.
[110]
S. Adriano, C. T. Angelo, D. Bartolomeo, and X. Cristos, “Influence of water deficit and rewatering on the components of the ascorbate-glutathione cycle in four interspecific Prunus hybrids,” Plant Science, vol. 169, no. 2, pp. 403–412, 2005.
[111]
N. Dipierro, D. Mondelli, C. Paciolla, G. Brunetti, and S. Dipierro, “Changes in the ascorbate system in the response of pumpkin (Cucurbita pepo L.) roots to aluminium stress,” Journal of Plant Physiology, vol. 162, no. 5, pp. 529–536, 2005.
[112]
C. Barth, W. Moeder, D. F. Klessig, and P. L. Conklin, “The timing of senescence and response to pathogens is altered in the ascorbate-deficient arabidopsis mutant vitamin c-1,” Plant Physiology, vol. 134, no. 4, pp. 1784–1792, 2004.
[113]
I. A. Graham and P. J. Eastmond, “Pathways of straight and branched chain fatty acid catabolism in higher plants,” Progress in Lipid Research, vol. 41, no. 2, pp. 156–181, 2002.
[114]
R. T. Mullen and R. N. Trelease, “Biogenesis and membrane properties of peroxisomes: does the boundary membrane serve and protect?” Trends in Plant Science, vol. 1, no. 11, pp. 389–394, 1996.
[115]
J. R. Bunkelmann and R. N. Trelease, “Ascorbate peroxidase: a prominent membrane protein in oilseed glyoxysomes,” Plant Physiology, vol. 110, no. 2, pp. 589–598, 1996.
[116]
K. Karyotou and R. P. Donaldson, “Ascorbate peroxidase, a scavenger of hydrogen peroxide in glyoxysomal membranes,” Archives of Biochemistry and Biophysics, vol. 434, no. 2, pp. 248–257, 2005.
[117]
K. Yamaguchi, H. Mori, and M. Nishimura, “A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin,” Plant and Cell Physiology, vol. 36, no. 6, pp. 1157–1162, 1995.
[118]
S. Narendra, S. Venkataramani, G. Shen et al., “The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development,” Journal of Experimental Botany, vol. 57, no. 12, pp. 3033–3042, 2006.
[119]
J. Wang, H. Zhang, and R. D. Allen, “Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress,” Plant and Cell Physiology, vol. 40, no. 7, pp. 725–732, 1999.
[120]
G. H. Badawi, N. Kawano, Y. Yamauchi et al., “Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit,” Physiologia Plantarum, vol. 121, no. 2, pp. 231–238, 2004.
[121]
P. J. Eastmond, “MONODEHYROASCORBATE REDUCTASE4 is required for seed storage oil hydrolysis and postgerminative growth in Arabidopsis,” Plant Cell, vol. 19, no. 4, pp. 1376–1387, 2007.
[122]
P. J. Eastmond, “SUGAR-DEPENDENT1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds,” Plant Cell, vol. 18, no. 3, pp. 665–675, 2006.
[123]
O. Arrigoni, M. B. Bitonti, R. Cozza, A. M. Innocenti, R. Liso, and R. Veltri, “Ascorbic acid effect on pericycle cell line in Allium cepa root,” Caryologia, vol. 42, pp. 213–216, 1989.
[124]
R. C. De Cabo, J. A. Gonzalez-Reyes, and P. Navas, “The onset of cell proliferation is stimulated by ascorbate free radical in onion root primordia,” Biology of the Cell, vol. 77, no. 2, pp. 231–233, 1993.
[125]
M. C. De Pinto, D. Francis, and L. De Gara, “The redox state of the ascorbate-dehydroascorbate pair as a specific sensor of cell division in tobacco BY-2 cells,” Protoplasma, vol. 209, no. 1-2, pp. 90–97, 1999.
[126]
A. M. Innocenti, M. B. Bitonti, O. Arrigoni, and R. Liso, “The size of quiescent centre in roots of Allium cepa L. grown with ascorbic acid,” New Phytologist, vol. 110, pp. 507–509, 1990.
[127]
R. Liso, A. M. Innocenti, M. B. Bitonti, and O. Arrigoni, “Ascorbic acid-induced progression of quiescent centre cells from G1 to S phase,” New Phytologist, vol. 110, pp. 469–471, 1988.
[128]
K. Tabata, K. ？ba, K. Suzuki, and M. Esaka, “Generation and properties of ascorbic acid-deficient transgenic tobacco cells expressing antisense RNA for L-galactono-1,4-lactone dehydrogenase,” Plant Journal, vol. 27, no. 2, pp. 139–148, 2001.
[129]
N. Kato and M. Esaka, “Changes in ascorbate oxidase gene expression and ascorbate levels in cell division and cell elongation in tobacco cells,” Physiologia Plantarum, vol. 105, no. 2, pp. 321–329, 1999.
[130]
G. Potters, N. Horemans, S. Bellone et al., “Dehydroascorbate influences the plant cell cycle through a glutathione-independent reduction mechanism,” Plant Physiology, vol. 134, no. 4, pp. 1479–1487, 2004.
[131]
G. Potters, N. Horemans, R. J. Caubergs, and H. Asard, “Ascorbate and dehydroascorbate influence cell cycle progression in a tobacco cell suspension,” Plant Physiology, vol. 124, no. 1, pp. 17–20, 2000.
[132]
O. Arrigoni, “Ascorbate system in plant development,” Journal of Bioenergetics and Biomembranes, vol. 26, no. 4, pp. 407–419, 1994.
[133]
S. Citterio, S. Sgorbati, S. Scippa, and E. Sparvoli, “Ascorbic acid effect on the onset of cell proliferation in pea root,” Physiologia Plantarum, vol. 92, no. 4, pp. 601–607, 1994.
[134]
R. Liso, G. Calabrese, M. B. Bitonti, and O. Arrigoni, “Relationship between ascorbic acid and cell division,” Experimental Cell Research, vol. 150, no. 2, pp. 314–320, 1984.
[135]
N. Horemans, G. Potters, L. De Wilde, and R. J. Caubergs, “Dehydroascorbate uptake activity correlates with cell growth and cell division of tobacco Bright Yellow-2 cell cultures,” Plant Physiology, vol. 133, no. 1, pp. 361–367, 2003.
[136]
G. Potters, L. De Gara, H. Asard, and N. Horemans, “Ascorbate and glutathione: guardians of the cell cycle, partners in crime?” Plant Physiology and Biochemistry, vol. 40, no. 6–8, pp. 537–548, 2002.
[137]
J. P. Reichheld, T. Vernoux, F. Lardon, M. van Montagu, and D. Inzé, “Specific checkpoints regulate plant cell cycle progression in response to oxidative stress,” Plant Journal, vol. 17, no. 6, pp. 647–656, 1999.
[138]
C. Paciolla, M. C. De Tullio, A. Chiappetta et al., “Short- and long-term effects of dehydroascorbate in Lupinus albus and Allium cepa roots,” Plant and Cell Physiology, vol. 42, no. 8, pp. 857–863, 2001.
[139]
M. J. May, T. Vernoux, C. Leaver, M. Van Montagu, and D. Inzé, “Glutathione homeostasis in plants: implications for environmental sensing and plant development,” Journal of Experimental Botany, vol. 49, no. 321, pp. 649–667, 1998.
[140]
M. C. De Tullio, C. Paciolla, F. Dalla Vecchia et al., “Changes in onion root development induced by the inhibition of peptidyl-prolyl hydroxylase and influence of the ascorbate system on cell division and elongation,” Planta, vol. 209, no. 4, pp. 424–434, 1999.
[141]
Z. Chen and D. R. Gallie, “Induction of monozygotic twinning by ascorbic acid in tobacco,” PLoS ONE, vol. 7, Article ID e39147, 2012.
[142]
O. Arrigoni, L. De Gara, F. Tommasi, and R. Liso, “Changes in the ascorbate system during seed development of Vicia faba L,” Plant Physiology, vol. 99, no. 1, pp. 235–238, 1992.
[143]
L. De Gara, M. C. De Pinto, and O. Arrigoni, “Ascorbate synthesis and ascorbate peroxidase activity during the early stage of wheat germination,” Physiologia Plantarum, vol. 100, no. 4, pp. 894–900, 1997.
[144]
F. Tommasi, C. Paciolla, M. C. De Pinto, and L. De Gara, “A comparative study of glutathione and ascorbate metabolism during germination of Pinus pinea L. seeds,” Journal of Experimental Botany, vol. 52, no. 361, pp. 1647–1654, 2001.
[145]
G. Borraccino, L. Mastropasqua, S. De Leonardis, and S. Dipierro, “The role of the ascorbic acid system in delaying the senescence of oat (Avena sativa L.) leaf segments,” Journal of Plant Physiology, vol. 144, no. 2, pp. 161–166, 1994.
[146]
Z. Chen and D. R. Gallie, “Dehydroascorbate reductase affects leaf growth, development, and function,” Plant Physiology, vol. 142, no. 2, pp. 775–787, 2006.
[147]
U. Takahama, M. Hirotsu, and T. Oniki, “Age-dependent changes in levels of ascorbic acid and chlorogenic acid, and activities of peroxidase and superoxide dismutase in the apoplast of tobacco leaves: mechanism of the oxidation of chlorogenic acid in the apoplast,” Plant and Cell Physiology, vol. 40, no. 7, pp. 716–724, 1999.
[148]
G. M. Pastori, G. Kiddle, J. Antoniw et al., “Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling,” Plant Cell, vol. 15, no. 4, pp. 939–951, 2003.
[149]
V. Pavet, E. Olmos, G. Kiddle et al., “Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis,” Plant Physiology, vol. 139, no. 3, pp. 1291–1303, 2005.
[150]
P. L. Conklin and C. Barth, “Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens, and the onset of senescence,” Plant, Cell and Environment, vol. 27, no. 8, pp. 959–970, 2004.
[151]
S. O. Kotchoni, K. E. Larrimore, M. Mukherjee, C. F. Kempinski, and C. Barth, “Alterations in the endogenous ascorbic acid content affect flowering time in Arabidopsis,” Plant Physiology, vol. 149, no. 2, pp. 803–815, 2009.
[152]
C. Barth, M. De Tullio, and P. L. Conklin, “The role of ascorbic acid in the control of flowering time and the onset of senescence,” Journal of Experimental Botany, vol. 57, no. 8, pp. 1657–1665, 2006.
[153]
S. M. Bulley, M. Rassam, D. Hoser et al., “Gene expression studies in kiwifruit and gene over-expression in Arabidopsis indicates that GDP-L-galactose guanyltransferase is a major control point of vitamin C biosynthesis,” Journal of Experimental Botany, vol. 60, no. 3, pp. 765–778, 2009.
[154]
M. M. Baig, S. Kelly, and F. Loewus, “L-Ascorbic acid biosynthesis in higher plants from L-gulono-1, 4-lactone and L-galactono-1, 4-lactone,” Plant Physiology, vol. 46, no. 2, pp. 277–280, 1970.
[155]
K. Oba, M. Fukui, Y. Imai, S. Iriyama, and K. Nogami, “L-Galactono-γ-lactone dehydrogenase: partial characterization, induction of activity and role in the synthesis of ascorbic acid in wounded white potato tuber tissue,” Plant and Cell Physiology, vol. 35, no. 3, pp. 473–478, 1994.
[156]
G. Noctor and C. H. Foyer, “Ascorbate and glutathione: keeping active oxygen under control,” Annual Review of Plant Biology, vol. 49, pp. 249–279, 1998.
[157]
N. Smirnoff, P. L. Conklin, and F. A. Loewus, “Biosynthesis of ascorbic acid in plants: a renaissance,” Annual Review of Plant Biology, vol. 52, pp. 437–467, 2001.
[158]
H. Yamasaki, S. Takahashi, and R. Heshiki, “The tropical fig Ficus microcarpa L. f. cv. Golden leaves lacks heat-stable dehydroascorbate reductase activity,” Plant and Cell Physiology, vol. 40, no. 6, pp. 640–646, 1999.
[159]
R. Mittler, S. Vanderauwera, M. Gollery, and F. Van Breusegem, “Reactive oxygen gene network of plants,” Trends in Plant Science, vol. 9, no. 10, pp. 490–498, 2004.
[160]
S. Yoshida, M. Tamaoki, T. Shikano et al., “Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana,” Plant and Cell Physiology, vol. 47, no. 2, pp. 304–308, 2006.
[161]
L. Rizhsky, H. Liang, and R. Mittler, “The water-water cycle is essential for chloroplast protection in the absence of stress,” Journal of Biological Chemistry, vol. 278, no. 40, pp. 38921–38925, 2003.
[162]
Z. Chen and D. R. Gallie, “Increasing tolerance to ozone by elevating foliar ascorbic acid confers greater protection against ozone than increasing avoidance,” Plant Physiology, vol. 138, no. 3, pp. 1673–1689, 2005.
[163]
B. C. B？nsager, A. Shahpiri, C. Finnie, and B. Svensson, “Proteomic and activity profiles of ascorbate-glutathione cycle enzymes in germinating barley embryo,” Phytochemistry, vol. 71, no. 14-15, pp. 1650–1656, 2010.
[164]
C. Yu, Y. Yang, X. Liu et al., “Molecular and biochemical analysis of two genes encoding dehydroascorbate reductase in common wheat,” Shengwu Gongcheng Xuebao/Chinese Journal of Biotechnology, vol. 25, no. 10, pp. 1483–1489, 2009.
[165]
J. Urano, T. Nakagawa, Y. Maki et al., “Molecular cloning and characterization of a rice dehydroascorbate reductase,” FEBS Letters, vol. 466, no. 1, pp. 107–111, 2000.
[166]
M. Secenji, E. Hideg, A. Bebes, and J. Gy？rgyey, “Transcriptional differences in gene families of the ascorbate-glutathione cycle in wheat during mild water deficit,” Plant Cell Reports, vol. 29, no. 1, pp. 37–50, 2009.
[167]
C. Neubauer and H. Y. Yamamoto, “Membrane barriers and Mehler-peroxidase reaction limit the ascorbate available for violaxanthin de-epoxidase activity in intact chloroplasts,” Photosynthesis Research, vol. 39, no. 2, pp. 137–147, 1994.
[168]
C. Miyake and K. Asada, “Ferredoxin-dependent photoreduction of the monodehydroascorbate radical in spinach thylakoids,” Plant and Cell Physiology, vol. 35, no. 4, pp. 539–549, 1994.
[169]
S. Sano, C. Miyake, B. Mikami, and K. Asada, “Molecular characterization of monodehydroascorbate radical reductase from cucumber highly expressed in Escherichia coli,” Journal of Biological Chemistry, vol. 270, no. 36, pp. 21354–21361, 1995.
[170]
L. Pnueli, H. Liang, M. Rozenberg, and R. Mittler, “Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants,” Plant Journal, vol. 34, no. 2, pp. 187–203, 2003.
[171]
A. Schützendübel, P. Nikolova, C. Rudolf, and A. Polle, “Cadmium and H2O2-induced oxidative stress in Populus x canescens roots,” Plant Physiology and Biochemistry, vol. 40, no. 6–8, pp. 577–584, 2002.
[172]
A. Schützendübel, P. Schwanz, T. Teichmann et al., “Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots,” Plant Physiology, vol. 127, no. 3, pp. 887–898, 2001.
[173]
P. Sharma and R. Shanker Dubey, “Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: role of osmolytes as enzyme protectant,” Journal of Plant Physiology, vol. 162, no. 8, pp. 854–864, 2005.
[174]
A. Jiménez, J. A. Hernández, L. A. del Río, and F. Sevilla, “Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves,” Plant Physiology, vol. 114, no. 1, pp. 275–284, 1997.
[175]
K. Obara, K. Sumi, and H. Fukuda, “The use of multiple transcription starts causes the dual targeting of Arabidopsis putative monodehydroascorbate reductase to both mitochondria and chloroplasts,” Plant and Cell Physiology, vol. 43, no. 7, pp. 697–705, 2002.
[176]
C. S. Lisenbee, M. J. Lingard, and R. N. Trelease, “Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase,” Plant Journal, vol. 43, no. 6, pp. 900–914, 2005.
[177]
M. Leterrier, F. J. Corpas, J. B. Barroso, L. M. Sandalio, and L. A. Del Río, “Peroxisomal monodehydroascorbate reductase. Genomic clone characterization and functional analysis under environmental stress conditions,” Plant Physiology, vol. 138, no. 4, pp. 2111–2123, 2005.
[178]
Z. Chen and D. R. Gallie, “The ascorbic acid redox state controls guard cell signaling and stomatal movement,” Plant Cell, vol. 16, no. 5, pp. 1143–1162, 2004.
[179]
S. Y. Kwon, Y. O. Ahn, H. S. Lee, and S. S. Kwak, “Biochemical characterization of transgenic tobacco plants expressing a human dehydroascorbate reductase gene,” Journal of Biochemistry and Molecular Biology, vol. 34, no. 4, pp. 316–321, 2001.
[180]
S. Y. Kwon, S. M. Choi, Y. O. Ahn et al., “Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbate reductase gene,” Journal of Plant Physiology, vol. 160, no. 4, pp. 347–353, 2003.
[181]
Z. Chen and D. R. Gallie, “Dehydroascorbate reductase affects non-photochemical quenching and photosynthetic performance,” Journal of Biological Chemistry, vol. 283, no. 31, pp. 21347–21361, 2008.
[182]
A. E. Eltayeb, N. Kawano, G. H. Badawi et al., “Enhanced tolerance to ozone and drought stresses in transgenic tobacco overexpressing dehydroascorbate reductase in cytosol,” Physiologia Plantarum, vol. 127, no. 1, pp. 57–65, 2006.
[183]
L. Yin, S. Wang, A. E. Eltayeb et al., “Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to Aluminum stress in transgenic Tobacco,” Planta, vol. 231, no. 3, pp. 609–621, 2010.
[184]
B. Le Martret, M. Poage, K. Shiel, G. D. Nugent, and P. J. Dix, “Tobacco chloroplast transformants expressing genes encoding dehydroascorbate reductase, glutathione reductase, and glutathione-S-transferase, exhibit altered anti-oxidant metabolism and improved abiotic stress tolerance,” Plant Biotechnology Journal, vol. 9, no. 6, pp. 661–673, 2011.
[185]
Y.-M. Goo, J.-C. Hyun, T.-W. Kim et al., “Expressional characterization of dehydroascorbate reductase cDNA in transgenic potato plants,” Journal of Plant Biology, vol. 51, no. 1, pp. 35–41, 2008.
[186]
A. Qin, Q. Shi, and X. Yu, “Ascorbic acid contents in transgenic potato plants overexpressing two dehydroascorbate reductase genes,” Molecular Biology Reports, vol. 38, no. 3, pp. 1557–1566, 2011.
[187]
Z. Wang, Y. Xiao, W. Chen, K. Tang, and L. Zhang, “Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis,” Journal of Integrative Plant Biology, vol. 52, no. 4, pp. 400–409, 2010.
[188]
T. Ushimaru, T. Nakagawa, Y. Fujioka et al., “Transgenic Arabidopsis plants expressing the rice dehydroascorbate reductase gene are resistant to salt stress,” Journal of Plant Physiology, vol. 163, no. 11, pp. 1179–1184, 2006.
[189]
V. M. Haroldsen, C. L. Chi-Ham, S. Kulkarni, A. Lorence, and A. B. Bennett, “Constitutively expressed DHAR and MDHAR influence fruit, but not foliar ascorbate levels in tomato,” Plant Physiology and Biochemistry, vol. 49, pp. 1244–1249, 2011.
[190]
R. Stevens, D. Page, B. Gouble, C. Garchery, D. Zamir, and M. Causse, “Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress,” Plant, Cell and Environment, vol. 31, no. 8, pp. 1086–1096, 2008.
[191]
A. E. Eltayeb, N. Kawano, G. H. Badawi et al., “Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses,” Planta, vol. 225, no. 5, pp. 1255–1264, 2007.
[192]
F. Li, Q. Y. Wu, Y. L. Sun, L. Y. Wang, X. H. Yang, and Q. W. Meng, “Overexpression of chloroplastic monodehydroascorbate reductase enhanced tolerance to temperature and methyl viologen-mediated oxidative stresses,” Physiologia Plantarum, vol. 139, no. 4, pp. 421–434, 2010.
[193]
M. Sanmartin, P. D. Drogoudi, T. Lyons, I. Pateraki, J. Barnes, and A. K. Kanellis, “Over-expression of ascorbate oxidase in the apoplast of transgenic tobacco results in altered ascorbate and glutathione redox states and increased sensitivity to ozone,” Planta, vol. 216, no. 6, pp. 918–928, 2003.
[194]
G. E. Taylor Jr., “Plant and leaf resistance to gaseous air pollution stress,” New Phytologist, vol. 80, pp. 523–534, 1978.
[195]
H. D. Grimes, K. K. Perkins, and W. F. Boss, “Ozone degrades into hydroxyl radical under physiological conditions. A spin trapping study,” Plant Physiology, vol. 72, no. 4, pp. 1016–1020, 1983.
[196]
J. H. Joo, S. Wang, J. G. Chen, A. M. Jones, and N. V. Fedoroff, “Different signaling and cell death roles of heterotrimeric G protein α and β subunits in the Arabidopsis oxidative stress response to ozone,” Plant Cell, vol. 17, no. 3, pp. 957–970, 2005.
[197]
Y. K. Sharma and K. R. Davis, “The effects of ozone on antioxidant responses in plants,” Free Radical Biology and Medicine, vol. 23, no. 3, pp. 480–488, 1997.
[198]
K. Tanaka, Y. Suda, N. Kondo, and K. Sugahara, “O3 tolerance and the ascorbate-dependent H2O2 decomposing system in chloroplasts,” Plant and Cell Physiology, vol. 26, no. 7, pp. 1425–1431, 1985.
[199]
Y. P. Lee, S. H. Kim, J. W. Bang, H. S. Lee, S. S. Kwak, and S. Y. Kwon, “Enhanced tolerance to oxidative stress in transgenic tobacco plants expressing three antioxidant enzymes in chloroplasts,” Plant Cell Reports, vol. 26, no. 5, pp. 591–598, 2007.
[200]
A. Yamamoto, M. N. H. Bhuiyan, R. Waditee et al., “Suppressed expression of the apoplastic ascorbate oxidase gene increases salt tolerance in tobacco and Arabidopsis plants,” Journal of Experimental Botany, vol. 56, no. 417, pp. 1785–1796, 2005.
[201]
S. M. Assmann and X. Q. Wang, “From milliseconds to millions of years: guard cells and environmental responses,” Current Opinion in Plant Biology, vol. 4, no. 5, pp. 421–428, 2001.
[202]
J. I. Schroeder, G. J. Allen, V. Hugouvieux, J. M. Kwak, and D. Waner, “Guard cell signal transduction,” Annual Review of Plant Biology, vol. 52, pp. 627–658, 2001.
[203]
M. Alhagdow, F. Mounet, L. Gilbert et al., “Silencing of the mitochondrial ascorbate synthesizing enzyme L-galactono-1,4-lactone dehydrogenase affects plant and fruit development in tomato,” Plant Physiology, vol. 145, no. 4, pp. 1408–1422, 2007.
[204]
E. I. Urzica, L. N. Adler, M. D. Page et al., “Impact of oxidative stress on ascorbate biosynthesis in Chlamydomonas via regulation of the VTC2 gene encoding a GDP- L-galactose phosphorylase,” The Journal of Biological Chemistry, vol. 287, pp. 14234–14245, 2012.
[205]
G. Kiddle, G. M. Pastori, S. Bernard et al., “Effects of leaf ascorbate content on defense and photosynthesis gene expression in Arabidopsis thaliana,” Antioxidants and Redox Signaling, vol. 5, no. 1, pp. 23–32, 2003.
