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Research Article

Metabolic Engineering of Plant L-Ascorbic Acid Biosynthesis: Recent Trends and Applications

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Pages 173-182 | Published online: 10 Oct 2008

REFERENCES

  • Asada K. Ascorbate peroxidase: a hydrogen peroxide-scavenging enzyme in plants. Physiol. Plant. 1992; 85: 235–241
  • Asard H., May J. M., Smirnoff N. Vitamin C Function and Biochemistry in Animals and Plants. Bios Scientific Publishers, London 2004
  • Baier M., Noctor G., Foyer C. H., Karl-Josef Dietz K. J. Antisense suppression of 2-cysteine peroxiredoxin in arabidopsis specifically enhances the activities and expression of enzymes associated with ascorbate metabolism but not glutathione metabolism. Plant Physiol. 2000; 124: 823–832
  • Barber G. A. The synthesis of L-galactose by plant enzyme systems. Arch. Biochem. Biophys. 1971; 147: 619–623
  • Barber G. A. Observations on the mechanism of the reversible epimerization of GDP-D-mannose to GDP-L-galactose by an enzyme from Chlorella pyrenoidosa. J. Biol. Chem. 1979; 254: 7600–7603
  • Berry A., Running J., Severson D. K., Burlingame R. P. Vitamin C production in microorganisms and plants. International Patent Application, WO99/64618, 1999
  • Boudrant J. Microbial processes for ascorbic acid biosynthesis: a review. Enzyme Microb. Technol. 1990; 12: 322–329
  • Burns J. J. Ascorbic acid. Metabolic Pathways, 3rd Ed, D. M. Greenberg. Academic Press, New York 1967; Vol. 1
  • Chen Z., Young T. E., Ling J., Chang S. C., Gallie D. R. Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc. Natl. Acad. Sci. USA 2003; 100: 3525–3530
  • Chen Z., Gallie D. R. Increasing tolerance to ozone by elevating foliar ascorbic acid confers greater protection against ozone than increasing avoidance. Plant Physiol. 2005; 138: 1673–1689
  • Chotani G., Dodge T., Hsu A., Kumar M., LaDuca R., Trimbur D., Weyler W., Sanford K. The commercial production of chemicals using pathway engineering. Biochim. Biophys. Acta 2000; 1543: 434–455
  • Conklin P. L. Recent advances in the role and biosynthesis of ascorbic acid in plants. Plant Cell Environ 2001; 24: 383–394
  • Conklin P. L., Gatzek S., Wheeler G. L., Dowdle J., Raymond M. J., Rolinski S., Isupov M., Littlechild J. A., Smirnoff N. Arabidopsis thaliana VTC4 encodes L-galactose 1-phosphate phosphatase, a plant ascorbic acid biosynthetic enzyme. J. Biol. Chem. 2006; 281: 15662–15670
  • Conklin P. L., Nprris S. R., Wheeler G. L., Williams E. H., Smirnoff N., Last R. L. Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. Proc. Natl. Acad. Sci. USA 1999; 96: 4198–4203
  • Conklin P. L., Pallanca J. E., Last R. L., Smirnoff N. L-Ascorbic acid metabolism in the ascorbate-deficient arabidopsis mutant vtc1. Plant Physiol. 1997; 115: 1277–1285
  • Cordenunsi B. R., Nascimento J. R. O., Genovese M. I., Lajolo F. M. Influence of cultivar on quality parameters and chemical composition of strawberry fruits grown in Brazil. J. Agric. Food Chem. 2002; 50: 2581–2586
  • Davey M. W., Van Montagu M., Inze D., Sanmartin M., Kanellis A., Smirnoff N., Benzie I. J. J., Strain J. J., Favell D., Fletcher J. Plant L-ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. J. Sci. Food Agric. 2000; 80: 825–860
  • Davletova S., Rizhsky L., Liang H. J., Zhong S. Q., Oliver D. J., Coutu J., Shulaev V., Schlauch K., Mittler R. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 2005; 17: 268–281
  • Doncheck J. A., Huss R. J., Running J. A., Skatrud T. J. L-ascorbic acid containing biomass of Chlorella pyrenoidosa. US Patent 5521090, 1996
  • Esaka M., Hattori T., Fujisawa K., Sakajo S., Asahi T. Molecular cloning and nucleotide sequence of full-length cDNA for ascorbate oxidase from cultured pumpkin cells. Eur. J. Biochem. 1990; 191: 537–541
  • Fernanda A., Rocío G. L., José L. C., Juan M. B., Miguel A. B., Victoriano V. Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase. Nat. Biotechnol. 2003; 21: 177–181
  • Franceschi V. R., Tarlyn N. M. L-ascorbic acid is accumulated in source leaf phloem and transported to sink tissues in plants. Plant Physiol 2002; 130: 649–656
  • Frey A. D., Oberle B. T., Farrés J., Kallio P. T. Expression of Vitreoscilla haemoglobin in tobacco cell cultures relieves nitrosative stress in vivo and protects from NO in vitro. Plant Biotechnol. J. 2004; 2: 221–231
  • Frykman S. A., Tsuruta H., Starks C. M., Regentin R., Carney J. R., Licari P. J. Control of secondary metabolite congener distributions via modulation of the dissolved oxygen tension. Biotechnol. Prog. 2002; 18: 913–920
  • Galtier N., Foyer C. H., Huber J., Voelker T. A., Huber S. C. Effects of elevated sucrose phosphate synthase activity on photosynthesis, assimilate partitioning, and growth in tomato (Lycoperscion esculentum var UC82B). Plant Physiol. 1993; 101: 535–543
  • Gatzek S., Wheeler G. L., Smirnoff N. 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 J. 2002; 30: 541–553
  • Green M. A., Fry S. C. Vitamin C degradation in plant cells via enzymatic hydrolysis of 4-O-oxalyl-L-threonate. Nature 2005; 433: 83–87
  • Hancock R. D., Viola R. Biotechnological approaches for L-ascorbic acid production. Trends Biotechnol. 2002; 20: 299–305
  • Harris J. R. Ascorbic Acid: Biochemistry and Biomedical Cell Biology, Subcellular Biochemistry. Plenum Press, New York 1996; Vol. 25
  • Heick H. M. C., Gra G. L. A., Humpers J. E. C. The occurrence of ascorbic acid among the yeasts. Can. J. Microbiol. 1969; 18: 597–600
  • Helsper J. P., Loewus F. A. Metabolism of l-Threonic Acid in Rumex x acutus L. and Pelargonium crispum (L.) L'Hér. Plant Physiol. 1982; 69: 1365–1368
  • Isherwood F. A. Synthesis of L-ascorbic acid in plants and animals. Biochem. J. 1954; 56: 1–15
  • Ishikawa T., Yoshimura K., Sakai K., Tamoi M., Takeda T., Shigeoka S. Molecular characterization and physiological role of a glyoxysome-bound ascorbate peroxidase from spinach. Plant Cell Physiol. 1998; 39: 23–34
  • Jain A. K., Nessler C. L. Metabolic engineering of an alternative pathway for ascorbic acid biosynthesis in plants. Mol. Breed. 2000; 6: 73–78
  • Kallio P. T., Kim D. J., Tsai P. S., Bailey J. E. Intracellular expression of Vitreoscilla hemoglobin alters Escherichia coli energy metabolism under oxygen-limited conditions. Eur. J. Biochem. 1994; 219: 201–208
  • Kappers I. F., Aharoni A., van Herpen T. W. J. M., Luckerhoff L. L. P., Dicke M., Bouwmeester H. J. Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 2005; 309: 2070–2072
  • Kato N., Esaka M. cDNA cloning and gene expression of ascorbate oxidase in tobacco. Plant Mol. Biol. 1996; 30: 833–837
  • Kato N., Esaka M. Changes in ascorbate oxidase gene expression and ascorbate level in cell division and cell elongation in tobacco cells. Physiol. Plant. 1999; 105: 321–329
  • Keller R., Renz F. S. A., Kossmann J. Antisense inhibition of the GDP-mannose pyrophosphorylase reduces the ascorbate content in transgenic plants leading to developmental changes during senescence. Plant J. 1999; 19: 131–141
  • Kisu Y., Harada Y., Goto M., Esaka M. Cloning of the pumpkin ascorbate oxidase gene and analysis of cis-acting region involved in induction by auxin. Plant Cell Physiol. 1997; 38: 631–637
  • Kwon S. Y., Choi S. M., Ahn Y. O., Lee H. S., Lee H. B., Park Y. M., Kwak S. S. Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbate reductase gene. J. Plant Physiol. 2003; 160: 347–353
  • Leech M. J., May K., Hallard D., Verpoorte R., de Luca V. Z., Christou P. Expression of two consecutive genes of a secondary metabolic pathway in transgenic tobacco: molecular diversity influences levels of expression and product accumulation. Plant Mol. Biol. 1998; 38: 765–774
  • Levin M. New concepts in the biology and biochemistry of ascorbic acid. N. Engl. J. Med. 1986; 314: 892–902
  • Lieman-Hurwitz J., Rachmilevitch S., Mittler R., Marcus Y., Kaplan A. Enhanced photosynthesis and growth of transgenic plants that express ictB, a gene involved in HCO3- accumulation in cyanobacteria. Plant Biotechnol. J. 2003; 1: 43–50
  • Lin L., Liu Y. G., Xu X. P., Li B. J. Efficient linking and transfer of multiple genes by a multigene assembly and transformation vector system. Proc. Natl. Acad. Sci. USA 2003; 100: 5962–5967
  • Lin L., Varner J. E. Expression of ascorbic acid oxidase in zucchini squash (Cucurbita pepo L.). Plant Physiol. 1991; 96: 159–165
  • Loewus F. A., Kelly S. Identity of L-ascorbic acid formed from D-glucose by the strawberry (Fragaria). Nature 1961; 191: 1059–1061
  • Lorence A., Chevone B. I., Mendes P., Nessler C. L. Myo-inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiol. 2004; 134: 1200–1205
  • Millar A. H., Mittova V., Kiddle G., Heazlewood J. L., Bartoli C. G., Theodoulou F. L., Foyer C. H. Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol. 2003; 133: 443–447
  • Mittler R., Herr E. H., Orvar B. L., van Camp W., Willekens H., Inzé D., Ellis B. E. Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyper responsive to pathogen infection. Proc. Natl. Acad. Sci. USA 1999; 96: 14165–1417
  • Miyagawa Y., Tamoi M., Shigeoka S. Overexpression of a cyanobacterial fructose-1,6-sedoheptulose-1,7-bisphosphatase in tobacco enhances photosynthesis and growth. Nat Biotechnol. 2001; 19: 965–969
  • Miyake C., Asada K. Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol. 1992; 33: 541–553
  • Mutsuda M., Ishikawa T., Takeda T., Shigeoka S. Subcellular localization and properties of l-galactono-γ -lactone dehydrogenase in spinach leaves. Biosci. Biotechnol. Biochem. 1995; 59: 1983–1984
  • Nascimento J. R. O., Higuchi B. K., Gómez M. L. P. A., Oshiro R. A., Lajolo F. M. L-ascorbate biosynthesis in strawberries: l-galactono-1,4-lactone dehydrogenase expression during fruit development and ripening. Postharvest Biol. Technol. 2005; 38: 34–42
  • Nishikimi M., Fukuyama R., Minoshima S., Shimizu N., Yagi K. Cloning and chromosome mapping of the human nonfunctional gene for L-gulono-lamma-lactone oxidase, the enzyme for L-ascorbic acid biosynthesis missing in man. J. Biol. Chem. 1994; 269: 13685–13688
  • Noctor G., Foyer C. H. Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998; 49: 249–279
  • Nunes-Nesi A., Carrari F., Lytovchenko A., Smith A. M. O., Loureiro M. E., Ratcliffe R. G., Sweetlove L. J., Fernie A. R. Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiol. 2005; 137: 611–622
  • Ôba K., Fukui M., Imai Y., Iriyama S., Nogami K. L-galactono-1,4-lactone dehydrogenase: partial characterization, induction of activity and role in the synthesis of ascorbic acid in wounded white potato tuber tissue. Plant Cell Physiol. 1994; 35: 473–478
  • Ôba K., Ishikawa S., Nishikawa M., Mizuno H., Yamamoto T. Purification and properties of L-galactono-γ -lactone dehydrogenase, a key enzyme for ascorbic acid biosynthesis, from sweet potato roots. J. Biochem. (Tokyo) 1995; 117: 120–124
  • Ohkawa J., Ohya T., Ito T., Nozawa H., Nishi Y., Okada N., Yoshida K., Takano M., Shinmyo A. Structure of the genomic DNA encoding cucumber ascorbate oxidase and its expression in transgenic plants. Plant Cell Rep. 1994; 13: 481–488
  • Oksman-Caldentey K. M., Inzé D. Plant cell factories in the post-genomic era: new ways to produce designer secondary metabolites. Trends Plant Sci. 2004; 9: 433–440
  • Örvar B. L., Ellis B. E. Transgenic tobacco plants expression antisense RNA for cytosolic ascorbate peroxidase show increased susceptibility to ozone injure. Plant J. 1997; 11: 1297–1305
  • Østergaard J., Persiau G., Davey M. W., Bauw G., van Montagu M. Isolation of a cDNA coding for L-galactono -gamma-lactone dehydrogenase, an enzyme involved in the biosynthesis of ascorbic acid in plants. J. Biol. Chem. 1997; 272: 30009–30016
  • Pfeifer B. A., Admiraal S. J., Gramajo H., Cane D. E., Khostla C. Biosynthesis of complex polyketides in a metabolic engineering stain of E. coli. Science 2001; 291: 1790–1792
  • Pignocchi C., Fletcher J. M., Wilkinson J. E., Barnes J. D., Foyer C. H. The function of ascorbate oxidase in tobacco. Plant Physiol. 2003; 132: 1631–1641
  • Running J. Process for the production of ascorbic acid with Prototheca. US Patent 5900370, 1999
  • Running J. A., Huss R. J., Olson P. T. Heterotrophic production of ascorbic acid by microalgae. J. Appl. Phycol. 1994; 6: 99–104
  • Saito K., Ohmoto J., Kuriha N. Incorporation of 18O into oxalic, l-threonic and l-tartaric acids during cleavage of l-ascorbic and 5-keto-d-gluconic acids in plants. Phytochemistry 1997; 44: 805–809
  • Sato F., Hashimoto T., Hachiya A., Tamura K., Choi K. B., Morishige T., Fujimoto H., Yamada Y. Metabolic engineering of plant alkaloid biosynthesis. Proc. Natl. Acad. Sci. USA 2001; 98: 367–372
  • Sauer M., Branduardi P., Valli M., Porro D. Production of L-ascorbic acid by metabolically engineered Saccharomyces cerevisiae Zygosaccharomyces bailii. Appl. Environ. Microbiol. 2004; 70: 6086–6091
  • Shimaoka T., Yokota A., Miyake C. Purification and characterization of chloroplast dehydroascorbate reductase from spinach leaves. Plant Cell Physiol. 2000; 41: 1110–1118
  • Skatrud T. J., Huss R. J. L-Ascorbic acid production in microorganisms. US Patent 5001059, 1991
  • Smirnoff N. The function and metabolism of ascorbic acid in plants. Ann. Bot. 1996; 78: 661–669
  • Smirnoff N., Conklin P. L., Loewus F. A. Biosynthesis of ascorbic acid in plants: a renaissance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001; 52: 437–467
  • Smirnoff N., Pallanca J. E. Ascorbate metabolism in relation to oxidative stress. Biochem. Soc. Trans. 1996; 24: 472–478
  • Sweetlove L. J., Kossmann J., Riesmeier J. W., Trethewey R. N., Hill S. A. The control of source to sink carbon flux during tuber development in potato. Plant J. 1998; 15: 697–706
  • Tabata K., Ôba K., Suzuki K., Esaka M. Generation and properties of ascorbic acid-deficient transgenic tobacco cells expressing antisense RNA for l-galactono 1,4-lactone dehydrogenase. Plant J. 2001; 27: 139–148
  • Tudela J. A., Hernández J. A., Gil M. A., Espín J. C. L-galactono-gamma-lactone dehydrogenase and vitamin C content in fresh-cut potatoes stored under controlled atmospheres. J. Agric. Food Chem. 2003; 51: 4296–4302
  • Verpoorte R., Memelink J. Engineering secondary metabolite production in plants. Curr. Opin. Biotechnol. 2002; 13: 181–187
  • Washko P. W., Welch R. W., Dhariwal K. R., Wang Y., Levine M. Ascorbic acid and dehydroascorbic acid analyses in biological samples. Anal. Biochem. 1992; 204: 1–14
  • Wheeler G. L., Jones M. A., Smirnoff N. The biosynthetic pathway of vitamin C in higher plants. Nature 1998; 393: 365–369
  • Wolucka B. A., Persiau G., Doorsselaere J. V., Davey M. W., Demol H., Vandekerckhove J., Montagu M. V., Zabeau M., Wout Boerjan W. Partial purification and identification of GDP-mannose 3′,5′-epimerase of Arabidopsis thaliana, a key enzyme of the plant vitamin C pathway. Proc. Natl. Acad. Sci. USA 2001; 98: 14843–14848
  • Yang J. C., Loewus F. A. Metabolic conversion of L-ascorbic-acid to oxalic-acid in oxalate accumulating plants. Plant Physiol. 1975; 56: 283–285
  • Zhang L., Ding R. X., Chai Y. R., Bonfill M., Moyano E., Oksman-Caldentey K. M., Xu T. F., Pi Y., Wang Z. N., Zhang H. M., Kai G. Y., Liao Z. H., Sun X. F., Tang K. X. Engineering tropane biosynthetic pathway in Hyoscyamus niger hairy root cultures. Proc. Natl. Acad. Sci. USA 2004; 101: 6786–6791

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