Vitamins B6-, C-, and E-Enriched Crops

  • Manish Sainger
  • Darshna Chaudhary
  • Ranjana Jaiwal
  • Anil K. Chhillar
  • Pawan Kumar JaiwalEmail author
Part of the Concepts and Strategies in Plant Sciences book series (CSPS)


Bourgeoning population and global climate change have put a tough challenge of feeding a large number of undernourished (with insufficient calorie intake) and malnourished (with limited or no access to essential micronutrients, vitamins, and minerals, causing the so-called hidden hunger) people globally. During the last few decades, the increase in production of calorie-rich staple food crops has resulted in a decrease in the number of undernourished people from over 1 billion to less than 800 million. However, no such equivalent increase in the production of non-staple foods (pulses, vegetables, fruits, and animal products) has been seen. The micronutrient malnutrition is still affecting more than 2 billion people or one-in-three people globally. Further, staple food crops are poor in vitamins that are further lost during storage, processing, and cooking. Vitamin deficiencies are prevalent in people who are solely dependent on staple crops for their diet and cannot afford diversified diet and have limited access to supplementation (multivitamin pills) or fortified food (addition of vitamins to food). Vitamin deficiencies in human cause severe physical and mental damages and are associated with enormous economic losses. Biofortification is a cost-effective and sustainable alternative to enhance vitamins in edible parts of the plant through breeding or metabolic engineering. The present chapter focuses on three relevant vitamins, B6, C, and E. An overview of their role in plants, metabolism, rational behind biofortification, and advances in manipulation of their contents in plants by the maker-assisted selection and metabolic engineering is presented.


Vitamins Metabolism Biofortification Vitamin B6 Ascorbate Tocochromanols 



MS and PKJ are thankful to DST-SERB, New Delhi, and UGC, New Delhi, for the award of Young Scientist fellowship (SB/YS/LS-190/2014) and BSR Faculty Fellowship (18-1/2011), respectively.


  1. Agius F, González-Lamothe R, Caballero JL, Muñoz-Blanco J, Botella MA et al (2003) Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase. Nat Biotechnol 21:177–181CrossRefGoogle Scholar
  2. Almeida J, Quadrana L, Asıs R, Setta N, de Godoy F, Bermudez L, Otaiza SN, Correada SJV, Fernie AR, Carrari F, Rossi M (2011) Genetic dissection of vitamin E biosynthesis in tomato. J Exp Bot 62:3781–3798CrossRefPubMedPubMedCentralGoogle Scholar
  3. Almeida J, Azevedo MS, Spicher L, Glauser G, Dorp K, Guyer L, Carranza AV et al (2016) Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner. J Exp Bot 67:919–934CrossRefGoogle Scholar
  4. Amaya I, Osorio S, Martinez-Ferri E, Lima-Silva V, Doblas VG, Fernández M, Valpuesta V et al (2015) Increased antioxidant capacity in tomato by ectopic expression of the strawberry D-galacturonate reductase gene. Biotechnol J 10:490–500CrossRefGoogle Scholar
  5. Asensi-Fabado MA, Munné-Bosch S (2010) Vitamins in plants: occurrence, biosynthesis and antioxidant function. Trends Plant Sci 15:582–592CrossRefGoogle Scholar
  6. Augustin J, Johnson SR, Teitzel C, Toma RB, Shaw RL, True RH et al (1978) Vitamin composition of freshly harvested and stored potatoes. J Food Sci 43:1566–1574CrossRefGoogle Scholar
  7. Austria R, Semenzato A, Bettero A (1997) Stability of vitamin C derivatives in solution and topical formulations. J Pharm Biomed Anal 15:795–801Google Scholar
  8. Badejo AA, Eltelib HA, Fujikawa Y, Esaka M (2009) Genetic manipulation for enhancing vitamin C content in tobacco expressing acerola (Malpighia glabra) GDP-l-galactose phosphorylase gene. Hortic Environ Biotechnol 50:329–333Google Scholar
  9. Badejo AA, Wada K, Gao Y, Maruta T, Sawa Y, Shigeoka S et al (2012) 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. J Exp Bot 63:229–239CrossRefGoogle Scholar
  10. Bagri DS, Upadhyaya DC, Kumar A, Upadhyaya CP (2018) Overexpression of PDX-II gene in potato (Solanum tuberosum L.) leads to the enhanced accumulation of vitamin B6 in tuber tissues and tolerance to abiotic stresses. Plant Sci 272:267–275CrossRefGoogle Scholar
  11. Bao G, Zhuo C, Qian C, Xiao T, Guo Z, Lu S (2016) Co-expression of NCED and ALO improves vitamin C level and tolerance to drought and chilling in transgenic tobacco and stylo plants. Plant Biotechnol J 14:206–214CrossRefGoogle Scholar
  12. Bilski P, Li MY, Ehrenshaft M, Daub ME, Chignell CF (2000) Vitamin B6 (pyridoxine) and its derivatives are efficient singlet oxygen quenchers and potential fungal antioxidants. J Photochem Photobiol 71:129–134Google Scholar
  13. Brigelius-Flohé R (2009) Vitamin E: the shrew waiting to be tamed. Free Radic Biol Med 46:543–554CrossRefGoogle Scholar
  14. Brummel DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–340Google Scholar
  15. Bulley S, Laing W (2016) The regulation of ascorbate biosynthesis. Curr Opin Plant Biol 33:15–22CrossRefGoogle Scholar
  16. Bulley SM, Rassam M, Hoser D, Otto W, Schuenemann N, Wright M et al (2009) Gene expression studies in kiwifruit and gene overexpression in Arabidopsis indicates that GDP-L-galactose guanyltransferase is a major control point of vitamin C biosynthesis. J Exp Bot 60:765–778CrossRefPubMedPubMedCentralGoogle Scholar
  17. Bulley S, Wright M, Rommens C, Yan H, Rassam M, Lin-Wang K et al (2012) Enhancing ascorbate in fruits and tubers through over-expression of the l-galactose pathway gene GDP-l-galactose phosphorylase. Plant Biotechnol J 10:390–397CrossRefGoogle Scholar
  18. Cahoon EB, Hall SE, Ripp KG, Ganzke TS, Hitz WD, Coughlan SJ (2003) Metabolic redesign of vitamin E biosynthesis in plants for tocotrienol production and increased antioxidant content. Nat Biotechnol 21:1082–1087CrossRefGoogle Scholar
  19. Cai X, Ye J, Hu T, Zhang Y, Ye Z, Li H (2014) Genome-wide classification and expression analysis of nucleobase-ascorbate transporter (NAT) gene family in tomato. Plant Growth Regul 73:19–30CrossRefGoogle Scholar
  20. Cai X, Zhang C, Ye J, Hu T, Ye Z, Li H, Zhang Y (2015) Ectopic expression of FaGalUR leads to ascorbate accumulation with enhanced oxidative stress, cold, and salt tolerance in tomato. Plant Growth Regul 76:187–197CrossRefGoogle Scholar
  21. Cai X, Zhang C, Shu W, Ye Z, Li H, Zhang Y (2016) The transcription factor SlDof22 involved in ascorbate accumulation and salinity stress in tomato. Biochem Biophys Res Commun 474:736–741CrossRefGoogle Scholar
  22. Caretto S, Nisi R, Paradiso A, De Gara L (2010) Tocopherol production in plant cell cultures. Mol Nutr Food Res 54:726–730CrossRefGoogle Scholar
  23. Carr AC, Frei B (1999) Toward a new recommended dietary allowance for vitamin C based on antioxidant and health effects in humans. Am J Clin Nutr 69:1086–1107Google Scholar
  24. Cellini B, Montioli R, Oppici E, Astegno A, Voltattorni CB (2014) The chaperone role of the pyridoxal 5′-phosphate and its implications for rare diseases involving B6-dependent enzymes. Clin Biochem 47:158–165CrossRefGoogle Scholar
  25. Chander S, Guo YQ, Yang XH, Yan JB, Zhang YR, Song TM, Li JS (2008) Genetic dissection of tocopherol content and composition in maize grain using quantitative trait loci analysis and the candidate gene approach. Mol Breed 22:353–365CrossRefGoogle Scholar
  26. Che P, Zhao ZY, Glassman K, Dolde D, Hu TX, Jones TJ, Albertsen MC (2016) Elevated vitamin E content improves all-trans β-carotene accumulation and stability in biofortified sorghum. Proc Natl Acad Sci USA 113:11040–11045CrossRefGoogle Scholar
  27. Chen Z, Gallie DR (2005) Increasing tolerance to ozone by elevating foliar ascorbic acid confers greater protection against ozone than increasing avoidance. Plant Physiol 138:1673–1689Google Scholar
  28. Chen H, Xiong LM (2009) Enhancement of vitamin B6 levels in seeds through metabolic engineering. Plant Biotechnol J 7:673–681CrossRefGoogle Scholar
  29. Chen Z, Young TE, Ling J, Chang SC, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci USA 100:3525–3530CrossRefGoogle Scholar
  30. Chen S, Li H, Liu G (2006) Progress of vitamin E metabolic engineering in plants. Trans Res 15:655–665Google Scholar
  31. Chen Z, Qin C, Lin L, Zeng X, Zhao Y, He S, Lu S, Guo Z (2015) Overexpression of yeast arabinono-1,4-lactone oxidase gene (ALO) increases tolerance to oxidative stress and Al toxicity in transgenic tobacco plants. Plant Mol Biol Rep 33:806–818CrossRefGoogle Scholar
  32. Cho EA, Lee CA, Kim YS, Baek SH, Reyes BG, Yun SJ (2005) Expression of γ-tocopherol methyltransferase transgene improves tocopherol composition in lettuce (Latuca sativa L.). Mol Cells (Springer Science & Business Media BV) 19(1)Google Scholar
  33. Cho KM, Nguyen HTK, Kim SY, Shin JS, Cho DH, Hong SB et al (2016) CML10, a variant of calmodulin, modulates ascorbic acid synthesis. New Phytol 209:664–678CrossRefGoogle Scholar
  34. Colinas M, Eisenhut M, Tohge T, Pesquera M, Fernie AR, Weber AP, Fitzpatrick TB (2016) Balancing of B6 vitamers is essential for plant development and metabolism in Arabidopsis. Plant Cell 28:439–453CrossRefPubMedPubMedCentralGoogle Scholar
  35. Collakova E, DellaPenna D (2003) Homogentisate phytyltransferase activity is limiting for tocopherol biosynthesis in Arabidopsis. Plant Physiol 131:632–642CrossRefPubMedPubMedCentralGoogle Scholar
  36. Conklin PL, Gatzek S, Wheeler GL, Dowdle J, Raymond MJ, Rolinski S et al (2006) Arabidopsis thaliana VTC4 encodes L-galactose-1-P phosphatase, a plant ascorbic acid biosynthetic enzyme. J Biol Chem 281:15662–15670CrossRefGoogle Scholar
  37. Conklin PL, DePaolo D, Wintle B, Schatz C, Buckenmeyer G (2013) Identification of Arabidopsis VTC3 as a putative and unique dual function protein kinase:protein phosphatase involved in the regulation of the ascorbic acid pool in plants. J Exp Bot 64:2793–2804CrossRefGoogle Scholar
  38. Cronje C, George GM, Fernie AR, Bekker J, Kossmann J, Bauer R (2012) Manipulation of L-ascorbic acid biosynthesis pathways in Solanum lycopersicum: elevated GDP-mannose pyrophosphorylase activity enhances L-ascorbate levels in red fruit. Planta 235:553–564CrossRefGoogle Scholar
  39. Cruz-Rus E, Botella MA, Valpuesta V, Gomez-Jimenez MC (2010) Analysis of genes involved in L-ascorbic acid biosynthesis during growth and ripening of grape berries. J Plant Physiol 167:739–748CrossRefGoogle Scholar
  40. DellaPenna D, Mene-Saffrane L (2011) Vitamin E. Adv Bot Res 59:179–227Google Scholar
  41. Di Salvo ML, Safo MK, Contestabile R (2012) Biomedical aspects of pyridoxal 5′-phosphate availability. Front Biosci 4:897–913Google Scholar
  42. Diepenbrock CH, Kandianis CB, Lipka AE, Magallanes-Lundback M, Vaillancourt B, Góngora-Castillo E, Ilut DC et al (2017) Novel loci underlie natural variation in vitamin E levels in maize grain. Plant Cell 29:2374–2392Google Scholar
  43. Dror DK, Allen LH (2011) Vitamin E deficiency in developing countries. Food Nutr Bull 32:124–143CrossRefGoogle Scholar
  44. El Airaj H, Gest N, Truffault V, Garchery C, Riqueau G, et al (2013) Decreased monodehydroascorbate reductase activity reduces tolerance to cold storage in tomato and affects fruit antioxidant levels. Postharvest Biol Technol 86:502–510Google Scholar
  45. Eltayeb AE, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Morishima I et al (2006) Enhanced tolerance to ozone and drought stresses in transgenic tobacco overexpressing dehydroascorbate reductase in cytosol. Physiol Plant 127:57–65CrossRefGoogle Scholar
  46. Endres S, Tenhaken R (2009) Myoinositol oxygenase controls the level of myoinositol in Arabidopsis, but does not increase ascorbic acid. Plant Physiol 149:1042–1049CrossRefPubMedPubMedCentralGoogle Scholar
  47. Evans HM, Emeeson OH, Emerson GA (1936) The isolation from wheat germ oil of an alcohol, α-tocopherol, having the properties of vitamin E. J Biol Chem 113:319–332Google Scholar
  48. Farre G, Sudhakar D, Naqvi S, Sandmann G, Christou P, Capell T et al (2012) Transgenic rice grains expressing a heterologous rhohydroxyphenylpyruvate dioxygenase shift tocopherol synthesis from the gamma to the alpha isoform without increasing absolute tocopherol levels. Transgenic Res 21:1093–1097CrossRefGoogle Scholar
  49. Fenech M, Amaya I, Valpuesta V, Botella MA (2019) Vitamin C content in fruits: biosynthesis and regulation. Front Plant Sci 9:2006CrossRefPubMedPubMedCentralGoogle Scholar
  50. Fernie AR, Tóth SZ (2015) Identification of the elusive chloroplast ascorbate transporter extends the substrate specificity of the PHT family. Mol Plant 8:674–676CrossRefGoogle Scholar
  51. Fitzpatrick TB, Amrhein N, Kappes B, Macheroux P, Tews I, Raschle T (2007) Two independent routes of de novo vitamin B6 biosynthesis: not that different after all. Biochem J 407:1–13CrossRefGoogle Scholar
  52. Fitzpatrick TB, Basset GJ, Borel P, Carrari F, DellaPenna D, Fraser PD et al (2012) Vitamin deficiencies in humans: can plant science help? Plant Cell 24:395–414CrossRefPubMedPubMedCentralGoogle Scholar
  53. Fotopoulos V, De Tullio MC, Barnes J, Kanellis AK (2008) Altered stomatal dynamics in ascorbate oxidase over-expressing tobacco plants suggest a role for dehydroascorbate signalling. J Exp Bot 59:729–737CrossRefGoogle Scholar
  54. Franceschi VR, Tarlyn NM (2002) L-ascorbic acid is accumulated in source leaf phloem and transported to sink tissues in plants. Plant Physiol 130:649–656CrossRefPubMedPubMedCentralGoogle Scholar
  55. Fraser PD, Enfissi EM, Halket JM, Truesdale MR, Yu D, Gerrish C, Bramley PM (2007) Manipulation of phytoene levels in tomato fruit: effects on isoprenoids, plastids, and intermediary metabolism. Plant Cell 19:3194–3211Google Scholar
  56. Frei B, Birlouez-Aragon I, Lykkesfeldt J (2012) Authors’ perspective: what is the optimum intake of vitamin C in humans? Crit Rev Food Sci Nutr 52:815–829CrossRefGoogle Scholar
  57. Fudge J, Mangel N, Gruissem W, Vanderschuren H, Fitzpatrick TB (2017) Rationalising vitamin B6 biofortification in crop plants. Curr Opin Biotechnol 44:130–137CrossRefGoogle Scholar
  58. Garcia-Casal MN, Peña-Rosas JP, Giyose B (2017) Staple crops biofortified with increased vitamins and minerals: considerations for a public health strategy. Ann NY Acad Sci 1390:3–13Google Scholar
  59. George GM, Ruckle ME, Abt MR, Bull SE (2017) Ascorbic Acid Biofortification in Crops. In: Hossain M, Munné-Bosch S, Burritt D, Diaz-Vivancos P, Fujita M, Lorence A (eds) Ascorbic acid in plant growth, development and stress tolerance. Springer, ChamGoogle Scholar
  60. Gest N, Gautier H, Stevens R (2013) Ascorbate as seen through plant evolution: the rise of a successful molecule? J Exp Bot 64:33–53CrossRefGoogle Scholar
  61. Ghavanini AA, Kimpinski K (2014) Revisiting the evidence for neuropathy caused by pyridoxine deficiency and excess. J Clin Neuromuscul Dis 16:25–31CrossRefGoogle Scholar
  62. Ghimire BK, Seong ES, Lee CO, Lim JD, Lee JG, Yoo JH et al (2011) Enhancement of alpha-tocopherol content in transgenic Perilla frutescens containing the gamma-TMT gene. Afr J Biotechnol 10:2430–2439Google Scholar
  63. Gilliland LU, Magallanes-Lundback M, Hemming C, Supplee A, Koornneef M, Bentsink L, DellaPenna D (2006) Genetic basis for natural variation in seed vitamin E levels in Arabidopsis thaliana. Proc Natl Acad Sci USA 103:18834–18841CrossRefGoogle Scholar
  64. Goo YM, Chun HJ, Kim TW, Lee CH, Ahn MJ, Bae SC, Lee SW et al (2008) Expressional characterization of dehydroascorbate reductase cDNA in transgenic potato plants. J Plant Biol 51:35–41Google Scholar
  65. Gregory JF III (2012) Accounting for differences in the bioactivity and bioavailability of vitamers. Food Nutr Res 56:5809CrossRefGoogle Scholar
  66. Grusak MA, DellaPenna D (1999) Improving the nutrient composition of plants to enhance human nutrition and health. Annu Rev Plant Biol 50:133–161Google Scholar
  67. Gutierrez-Gonzalez JJ, Garvin DF (2016) Subgenome-specific assembly of vitamin E biosynthesis genes and expression patterns during seed development provide insight into the evolution of oat genome. Plant Biotechnol J 14:2147–2157Google Scholar
  68. Haroldsen VM, Chi-Ham CL, Kulkarni S, Lorence A, Bennett AB (2011) Constitutively expressed DHAR and MDHAR influence fruit, but not foliar ascorbate levels in tomato. Plant Physiol Biochem 49:1244–1249CrossRefPubMedPubMedCentralGoogle Scholar
  69. Hass CG, Tang S, Leonard S, Traber MG, Miller JF, Knapp SJ (2006) Three non-allelic epistatically interacting methyltransferase mutations produce novel tocopherol (vitamin E) profiles in sunflower. Theor Appl Genet 113:767–778CrossRefGoogle Scholar
  70. Hellmann H, Mooney S (2010) Vitamin B6: a molecule for human health? Molecules 15:442–459Google Scholar
  71. Hemavathi U, Upadhyaya CP, Young KE, Akula N, Kim HS, Heung JJ, et al (2009) Over-expression of strawberry d-galacturonic acid reductase in potato leads to accumulation of vitamin C with enhanced abiotic stress tolerance. Plant Sci 177:659–667Google Scholar
  72. Herrero S, Daub ME (2007) Genetic manipulation of vitamin B6 biosynthesis in tobacco and fungi uncovers limitations to up-regulation of the pathway. Plant Sci 172:609–620CrossRefGoogle Scholar
  73. Herrero S, González E, Gillikin JW, Vélëz H, Daub ME (2011) Identification and characterization of a pyridoxal reductase involved in the vitamin B6 salvage pathway in Arabidopsis. Plant Mol Biol 76:157–169CrossRefGoogle Scholar
  74. Hey D, Rothbart M, Herbst J, Wang P, Müller J, Wittmann D, Gruhl K et al (2017) LIL3, a light-harvesting in Arabidopsis thaliana. Plant Physiol 174:1037–1050CrossRefPubMedPubMedCentralGoogle Scholar
  75. Hofius D, Hajirezaei MR, Geiger M, Tschiersch H, Melzer M, Sonnewald U (2004) RNAi-mediated tocopherol deficiency impairs photoassimilate export in transgenic potato plants. Plant Physiol 135:1256–1268Google Scholar
  76. Hu TX, Ye J, Tao PW, Li HX, Zhang JH, Zhang YY, Ye ZB (2016) The tomato HD-Zip I transcription factor SIHZ24 modulates ascorbate accumulation through positive regulation of the D-mannose/L-galactose pathway. Plant J 85:16–29CrossRefGoogle Scholar
  77. Imai T, Ban Y, Yamamoto T, Moriguchi T (2012) Ectopic overexpression of peach GDP-d-mannose pyrophosphorylase and GDP-d-mannose-3′, 5′-epimerase in transgenic tobacco. Plant Cell Tissue Organ Cult 111:1–13Google Scholar
  78. Ioannidi E, Kalamaki MS, Engineer C, Pateraki I, Alexandrou D, Mellidou I et al (2009) Expression profiling of ascorbic acid-related genes during tomato fruit development and ripening and in response to stress conditions. J Exp Bot 60:663–678CrossRefPubMedPubMedCentralGoogle Scholar
  79. Jain AK, Nessler CL (2000) Metabolic engineering of an alternative pathway for ascorbic acid biosynthesis in plants. Mol Breed 6:73–78CrossRefGoogle Scholar
  80. Jiang Q (2014) Natural forms of vitamin E: metabolism, antioxidant, and anti-inflammatory activities and their role in disease prevention and therapy. Free Radic Biol Med 72:76–90CrossRefPubMedPubMedCentralGoogle Scholar
  81. Justiniano R, Williams JD, Perer J, Hua A, Lesson J, Park SL et al (2017) The B6-vitamer pyridoxal is a sensitizer of UVA-induced genotoxic stress in human primary keratinocytes and reconstructed epidermis. Photochem Photobiol 93:990–998CrossRefPubMedPubMedCentralGoogle Scholar
  82. Kamal-Eldin A, Appelqvist LÅ (1996) The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids 31:671–701Google Scholar
  83. Kannappan R, Gupta SC, Kim JH, Aggarwal BB (2012) Tocotrienols fight cancer by targeting multiple cell signaling pathways. Genes Nutr 7:43Google Scholar
  84. Karunanandaa B, Qi Q, Hao M, Baszis SR, Jensen PK, Wong YH, Post-Beittenmiller D et al (2005) Metabolically engineered oilseed crops with enhanced seed tocopherol. Metab Eng 7:384–400CrossRefGoogle Scholar
  85. Kim YS, Kim IS, Bae MJ, Choe YH, Kim YH, Park HM et al (2013) Homologous expression of cytosolic dehydroascorbate reductase increases grain yield and biomass under paddy field conditions in transgenic rice (Oryza sativa L. japonica). Planta 237:1613–1625CrossRefGoogle Scholar
  86. Kulkarni S (2012) Elevating ascorbate content in tomato and studying the role of jasmonates in modulating ascorbate in Arabidopsis. MS thesis, Arkansas State University, Jonesboro, ARGoogle Scholar
  87. Laing WA, Wright MA, Cooney J, Bulley SM (2007) The missing step of the L-galactose pathway of ascorbate biosynthesis in plants, an L-galactose guanyltransferase, increases leaf ascorbate content. Proc Nat Acad Sci 104:9534–9539Google Scholar
  88. Laing WA, Martinez-Sanchez M, Wright MA, Bulley SM, Brewster D, Dare AP et al (2015) An upstream open reading frame is essential for feedback regulation of ascorbate biosynthesis in Arabidopsis. Plant Cell 27:772–786CrossRefPubMedPubMedCentralGoogle Scholar
  89. Landi M, Fambrini M, Basile A, Salvini M, Guidi L, Pugliesi C (2015) Overexpression of L-galactono-1, 4-lactone dehydrogenase (L-GalLDH) gene correlates with increased ascorbate concentration and reduced browning in leaves of Lactuca sativa L. after cutting. Plant Cell Tissue Organ Cult 123:109–120Google Scholar
  90. Li Y, Liu Y, Zhang J (2010a) Advances in the research on the AsA-GSH cycle in horticultural crops. Front Agric China 4:84–90Google Scholar
  91. Li F, Wu QY, Sun YL, Wang LY, Yang XH, Meng QW (2010b) Overexpression of chloroplastic monodehydroascorbate reductase enhanced tolerance to temperature and methyl viologen-mediated oxidative stresses. Physiol Plant 139:421–434PubMedGoogle Scholar
  92. Li Q, Li C, Yu X (2012a) Enhanced ascorbic acid accumulation through overexpression of dehydroascorbate reductase confers tolerance to methyl viologen & salt stresses in tomato. Czech J Genet Plant Breed 48:74–86CrossRefGoogle Scholar
  93. Li Q, Yang X, Xu S, Cai Y, Zhang D, Han Y, Yan J (2012b) Genome-wide association studies identified three independent polymorphisms associated with α-tocopherol content in maize kernels. PLoS ONE 7:e36807Google Scholar
  94. Li KT, Moulin M, Mangel N, Albersen M, Verhoeven-Duif NM, Ma QX et al (2015) Increased bioavailable vitamin B6 in field-grown transgenic cassava for dietary sufficiency. Nat Biotechnol 33:1029–1032PubMedGoogle Scholar
  95. Li S, Wang J, Yu Y, Wang F, Dong J, Huang R (2016) D27E mutation of VTC1 impairs the interaction with CSN5B and enhances ascorbic acid biosynthesis and seedling growth in Arabidopsis. Plant Mol Biol 92:473–482Google Scholar
  96. Li L, Lu M, An H (2017) Expression profiles of the genes involved in L-ascorbic acid biosynthesis and recycling in Rosa roxburghii leaves of various ages. Acta Physiol Plant 39:44–53CrossRefGoogle Scholar
  97. Li Y, Chu Z, Luo J, Zhou Y, Cai Y, Lu Y, Xia J, Kuang H, Ye Z, Ouyang B (2018a) The C2H2 zinc-finger protein SlZF3 regulates AsA synthesis and salt tolerance by interacting with CSN5B. Plant Biotechnol J 16:1201–1213CrossRefGoogle Scholar
  98. Li T, Yang X, Yu Y, Si X, Zhai X, Zhang H et al (2018b) Domestication of wild tomato is accelerated by genome editing. Nat Biotechnol.
  99. Liao P, Chen X, Wang M, Bach TJ, Chye ML (2018) Improved fruit α-tocopherol, carotenoid, squalene and phytosterol contents through manipulation of Brassica juncea 3-HYDROXY-3-METHYLGLUTARYL-COA SYNTHASE 1 in transgenic tomato. Plant Biotechnol J 16:784–796Google Scholar
  100. Lim MY, Pulla RK, Park JM, Harn CH, Jeong BR (2012) Overexpression of l-gulono-γ-lactone oxidase (GLOase) gene leads to ascorbate accumulation with enhanced abiotic stress tolerance in tomato. Cell Dev Biol Plant 48:453–461CrossRefGoogle Scholar
  101. Lim MY, Jeong BR, Jung M, Harn CH (2016) Transgenic tomato plants expressing strawberry d-galacturonic acid reductase gene display enhanced tolerance to abiotic stresses. Plant Biotechnol Rep 10:105–116CrossRefGoogle Scholar
  102. Lin YP, Wu MC, Chang YY (2016) Identification of a chlorophyll dephytylase involved in chlorophyll turnover in Arabidopsis. Plant Cell 28:2974–2990CrossRefPubMedPubMedCentralGoogle Scholar
  103. Lionetti V, Raiola A, Mattei B, Bellincampi D (2015) The grapevine VvPMEI1 gene encodes a novel functional pectin methylesterase inhibitor associated to grape berry development. PLoS ONE 10:e0133810. Scholar
  104. Lipka AE, Gore MA, Magallanes-Lundback M, Mesberg A, Lin H, Tiede T, DellaPenna D et al (2013) Genome-wide association study and pathway level analysis of tocochromanol levels in maize grain. G3 Genes Genomes Genet 3:1287–1299Google Scholar
  105. Lira BS, Rosado D, Almeida J, de Souza AP, Buckeridge MS, Purgatto E, Rossi M et al (2016) Pheophytinase knockdown impacts carbon metabolism and nutraceutical content under normal growth conditions in tomato. Plant Cell Physiol 57:642–653Google Scholar
  106. Lisko KA, Torres R, Harris RS, Belisle M, Vaughan MM, Jullian B et al (2013) Elevating vitamin C content via overexpression of myo-inositol oxygenase and L-gulono-1, 4-lactone oxidase in Arabidopsis leads to enhanced biomass and tolerance to abiotic stresses. In Vitro Cell Dev Biol-Plant 49:643–655CrossRefPubMedPubMedCentralGoogle Scholar
  107. Liu W, An H-M, Yang M (2013) Overexpression of Rosa roxburghii L-galactono-1,4-lactone dehydrogenase in tobacco plant enhances ascorbate accumulation and abiotic stress tolerance. Acta Physiol Plant 35:1617–1624CrossRefGoogle Scholar
  108. Liu F, Wang L, Gu L, Zhao W, Su H, Cheng X (2015) Higher transcription levels in ascorbic acid biosynthetic and recycling genes were associated with higher ascorbic acid accumulation in blueberry. Food Chem 188:399–405CrossRefGoogle Scholar
  109. Liu Y, Yang T, Lin Z, Guo B, Xing C, Zhao L, Huang X (2019) A WRKY transcription factor Pbr WRKY 53 from Pyrus betulaefolia is involved in drought tolerance and AsA accumulation. Plant Biotechnol J 17:1770–1787.
  110. Locato V, Cimini S, De Gara L (2014) Strategies to increase vitamin C in plants: from plant defense perspective to food biofortification. Front Plant Sci 4:1–12Google Scholar
  111. Loewus FA (1999) Biosynthesis and metabolism of ascorbic acid in plants and of analogs of ascorbic acid in fungi. Phytochemistry 52:193–210CrossRefGoogle Scholar
  112. Lorence A, Chevone BI, Mendes P, Nessler CL (2004) myo-inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiol 134:1200–1205CrossRefPubMedPubMedCentralGoogle Scholar
  113. Lu Y, Rijzaani H, Karcher D, Ruf S, Bock R (2013) Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons. Proc Natl Acad Sci USA 110:E623–E632Google Scholar
  114. Ma L, Wang Y, Liu W, Liu Z (2014) Overexpression of an alfalfa GDP-mannose 3,5-epimerase gene enhances acid, drought and salt tolerance in transgenic Arabidopsis by increasing ascorbate accumulation. Biotechnol Lett 36:2331–2341Google Scholar
  115. Macknight RC, Laing WA, Bulley SM, Broad RC, Johnson AA, Hellens RP (2017) Increasing ascorbate levels in crops to enhance human nutrition and plant abiotic stress tolerance. Curr Opin Biotechnol 44:153–160Google Scholar
  116. Mangel N, Fudge JB, Li KT, Wu TY, Tohge T et al (2019) Enhancement of vitamin B6 levels in rice expressing Arabidopsis vitamin B6 biosynthesis de novo genes. Plant J.
  117. Maruta T, Yonemitsu M, Yabuta Y, Tamoi M, Ishikawa T, Shigeoka S (2008) Arabidopsis phosphomannose isomerase 1, but not phosphomannose isomerase 2, is essential for ascorbic acid biosynthesis. J Biol Chem 283:28842–28851CrossRefPubMedPubMedCentralGoogle Scholar
  118. Mathur P, Ding Z, Saldeen T, Mehta JL (2015) Tocopherols in the prevention and treatment of atherosclerosis and related cardiovascular disease. Clin Cardiol 38:570–576Google Scholar
  119. Maurino VG, Grube E, Zielinski J, Schild A, Fischer K, Flügge UI (2006) Identification and expression analysis of twelve members of the nucleobase–ascorbate transporter (NAT) gene family in Arabidopsis thaliana. Plant Cell Physiol 47:1381–1393Google Scholar
  120. Mehansho H, Hamm MW, Henderson LM (1979) Transport and metabolism of pyridoxal and pyridoxal phosphate in the small intestine of the rat. J Nutr 109:1542–1551CrossRefGoogle Scholar
  121. Mellidou I, Kanellis AK (2017) Genetic control of ascorbic acid biosynthesis and recycling in horticultural crops. Front Chem 5:50CrossRefPubMedPubMedCentralGoogle Scholar
  122. Mellidou I, Chagné D, Laing WA, Keulemans J, Davey MW (2012) Allelic variation in paralogs of GDP-L-galactose phosphorylase is a major determinant of vitamin C concentrations in apple fruit. Plant Physiol 160:1613–1629CrossRefPubMedPubMedCentralGoogle Scholar
  123. Mène-Saffrané L (2018) Vitamin E biosynthesis and its regulation in plants. Antioxidants 7:2. Basel, SwitzerlandGoogle Scholar
  124. Mene-Saffrane L, Pellaud S (2017) Current strategies for vitamin E biofortification of crops. Curr Opin Biotechnol 44:189–197CrossRefGoogle Scholar
  125. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498CrossRefGoogle Scholar
  126. Miyaji T, Kuromori T, Takeuchi Y, Yamaji N, Yokosho K, Shimazawa A, Sugimoto E, Omote H, Ma JF, Shinozaki K, Moriyama Y (2015) AtPHT4;4 is a chloroplast-localized ascorbate transporter in Arabidopsis. Nat Commun 6:5928CrossRefPubMedPubMedCentralGoogle Scholar
  127. Mooney S, Chen LY, Kuhn C, Navarre R, Knowles NR, Hellmann H (2013) Genotype-specific changes in vitamin B6 content and the PDX family in potato. Biomed Res Int 2013:389723CrossRefPubMedPubMedCentralGoogle Scholar
  128. Moser MA, Chun OK (2016) Vitamin C and heart health: a review based on findings from epidemiologic studies. Int J Mol Sci 17:1328CrossRefPubMedPubMedCentralGoogle Scholar
  129. Mounet-Gilbert L, Dumont M, Ferrand C, Bournonville C, Monier A, Jorly J et al (2016) Two tomato GDP-D-mannose epimerase isoforms involved in ascorbate biosynthesis play specific roles in cell wall biosynthesis and development. J Exp Bot 67:4767–4777CrossRefPubMedPubMedCentralGoogle Scholar
  130. Munne-Bosch S, Falk J (2004) New insights into the function of tocopherols in plants. Planta 218:323–326CrossRefGoogle Scholar
  131. Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang Z, Costich DE, Buckler ES (2009) Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 21:2194–2202CrossRefPubMedPubMedCentralGoogle Scholar
  132. Naqvi S, Zhu C, Farre G, Ramessar K, Bassie L, Breitenbach J et al (2009) Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways. Proc Natl Acad Sci USA 106:7762–7767CrossRefGoogle Scholar
  133. Nunes-Nesi A, Carrari F, Lytovchenko A, Smith AM, Loureiro ME, Ratcliffe AG, Sweetlove LJ, Fernie AR (2005) Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiol 137:611–622CrossRefPubMedPubMedCentralGoogle Scholar
  134. Obol JH, Arony DA, Wanyama R, Moi KL, Bodo B, Odong PO, Odida M (2016) Reduced plasma concentrations of vitamin B6 and increased plasma concentrations of the neurotoxin 3-hydroxykynurenine are associated with nodding syndrome: a case control study in Gulu and Amuru districts, Northern Uganda. Pan Afr Med J 24:123CrossRefPubMedPubMedCentralGoogle Scholar
  135. Orvar BL, Ellis BE (1997) Transgenic tobacco plants expressing antisense RNA for cytosolic ascorbate peroxidases how increased susceptibility to ozone injury. Plant J 11:1297–1305CrossRefGoogle Scholar
  136. Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K et al (2007) The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 35:883–887CrossRefGoogle Scholar
  137. Pappenberger G, Hohmann HP (2014) Industrial production of L-ascorbic acid (vitamin C) and D-isoascorbic acid. Adv Biochem Eng Biotechnol 143:143–188PubMedGoogle Scholar
  138. Parra M, Stahl S, Hellmann H (2018) Vitamin B6 and its role in cell metabolism and physiology. Cells 7:84Google Scholar
  139. Pellaud S, Bory A, Chabert V, Romanens J, Chaisse-Leal L, Doan AV, Mène-Saffrané L (2018) WRINKLED 1 and ACYL-COA: DIACYLGLYCEROL ACYLTRANSFERASE 1 regulate tocochromanol metabolism in Arabidopsis. New Phytol 217:245–260Google Scholar
  140. Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase in tobacco. Plant Physiol 132:1631–1641CrossRefPubMedPubMedCentralGoogle Scholar
  141. Prochnik S, Marri PR, Desany B, Rabinowicz PD, Kodira C, Mohiuddin M et al (2012) The cassava genome: current progress, future directions. Trop Plant Biol 5:88–94CrossRefPubMedPubMedCentralGoogle Scholar
  142. Qian W, Yu C, Qin H, Liu X, Zhang A, Johansen IE et al (2007) Molecular and functional analysis of phosphomannomutase (PMM) from higher plants and genetic evidence for the involvement of PMM in ascorbic acid biosynthesis in Arabidopsis and Nicotiana benthamiana. Plant J 49:399–413CrossRefGoogle Scholar
  143. Qin A, Shi Q, Yu X (2011) Ascorbic acid contents in transgenic potato plants overexpressing two dehydroascorbate reductase genes. Mol Biol Rep 38:1557–1566CrossRefGoogle Scholar
  144. Qin A, Huang X, Zhang H, Wu J, Yang J, Zhang S (2015) Overexpression of PbDHAR2 from Pyrus sinkiangensis in transgenic tomato confers enhanced tolerance to salt and chilling stresses. HortScience 50:789–796Google Scholar
  145. Quadrana L, Almeida J, Otaiza SN, Duffy T, Da Silva JVC, de Godoy F, Rossi M (2013) Transcriptional regulation of tocopherol biosynthesis in tomato. Plant Mol Biol 81:309–325Google Scholar
  146. Quadrana L, Almeida J, Asís R, Duffy T, Dominguez PG, Bermúdez L, Asurmendi S (2014) Natural occurring epialleles determine vitamin E accumulation in tomato fruits. Nat Commun 5:4027CrossRefGoogle Scholar
  147. Radzio JA, Lorence A, Chevone BI, Nessler CL (2003) L-Gulono 1,4-lactone oxidase expression rescues vitamin C-deficient Arabidopsis (vtc) mutants. Plant Mol Biol 53:837–844CrossRefGoogle Scholar
  148. Raschke M, Boycheva S, Crèvecoeur M, Nunes-Nesi A, Witt S, Fernie AR et al (2011) Enhanced levels of vitamin B6 increase aerial organ size and positively affect stress tolerance in Arabidopsis. Plant J 66:414–432CrossRefGoogle Scholar
  149. Rigano MM, Lionetti V, Raiola A, Bellincampi D, Barone A et al (2018) Pectic enzymes as potential enhancers of ascorbic acid production through the D-galacturonate pathway in Solanaceae. Plant Sci 266:55–63CrossRefGoogle Scholar
  150. Rodríguez-Ruiz M, Mateos RM, Codesido V, Corpas FJ, Palma JM (2017) Characterization of the galactono-1,4-lactone dehydrogenase from pepper fruits and its modulation in the ascorbate biosynthesis. Role of nitric oxide. Redox Biol 12:171–181CrossRefPubMedPubMedCentralGoogle Scholar
  151. Römer S, Fraser PD, Kiano JW, Shipton CA, Misawa N, Schuch W, Bramley PM (2000) Elevation of the provitamin A content of transgenic tomato plants. Nat Biotechnol 18:666Google Scholar
  152. Roth-Maier DA, Kettler SI, Kirchgessner M (2002) Availability of vitamin B(6) from different food sources. Int J Food Sci Nutr 53:171–179CrossRefGoogle Scholar
  153. Ruggieri V, Sacco A, Calafiore R, Frusciante L, Barone A (2015) Dissecting a QTL into candidate genes highlighted the key role of pectinesterases in regulating the ascorbic acid content in tomato fruit. Plant Genome 8:1–10Google Scholar
  154. Sadre R, Gruber J, Frentzen M (2006) Characterization of homogentisate prenyltransferases involved in plastoquinone-9 and tocochromanol biosynthesis. FEBS Lett 580:5357–5362CrossRefGoogle Scholar
  155. Sang Y, Barbosa JM, Wu H, Locy RD, Singh NK (2007) Identification of a pyridoxine (pyridoxamine) 5′-phosphate oxidase from Arabidopsis thaliana. FEBS Lett 581:344–348CrossRefGoogle Scholar
  156. Sanmartin M, Drogoudi P, Lyons T, Pateraki I, Barnes J, Kanellis AK (2003) 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 216:918–928Google Scholar
  157. Sattler SE, Cheng Z, DellaPenna D (2004a) From Arabidopsis to agriculture: engineering improved Vitamin E content in soybean. Trends Plant Sci 9:365–367CrossRefGoogle Scholar
  158. Sattler SE, Gilliland LU, Magallanes-Lundback M, Pollard M, DellaPenna D (2004b) Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. Plant Cell 16:1419–1432Google Scholar
  159. Sauvage C, Segura V, Bauchet G, Stevens R, Do PT, Nikoloski Z et al (2014) Genome-wide association in tomato reveals 44 candidate loci for fruit metabolic traits. Plant Physiol 165:1120–1132CrossRefPubMedPubMedCentralGoogle Scholar
  160. Sawake S, Tajima N, Mortimer JC, Lao J, Ishikawa T, Yu X, Yamanashi Y et al (2015) KONJAC1 and 2 are key factors for GDP-mannose generation and affect l-ascorbic acid and glucomannan biosynthesis in Arabidopsis. Plant Cell 27:3397–3409CrossRefPubMedPubMedCentralGoogle Scholar
  161. Schauer N, Semel Y, Roessner U, Gur A, Balbo I, Carrari F, Willmitzer L (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol 24:447–454CrossRefGoogle Scholar
  162. Schwechheimer SK, Park EY, Revuelta JL, Becker J, Wittmann C (2016) Biotechnology of riboflavin. Appl Micro Biotechnol 100:2107–2119Google Scholar
  163. Seo YS, Kim SJ, Harn CH, Kim WT (2011) Ectopic expression of apple fruit homogentisate phytyltransferase gene (MdHPT1) increases tocopherol in transgenic tomato (Solanum lycopersicum cv. Micro-Tom) leaves and fruits. Phytochemistry 72:321–329CrossRefGoogle Scholar
  164. Shammugasamy B, Ramakrishnan Y, Ghazali HM, Muhammad K (2015) Tocopherol and tocotrienol contents of different varieties of rice in Malaysia. Sci Food Agric 95:672–678CrossRefGoogle Scholar
  165. Shintani D, DellaPenna D (1998) Elevating the vitamin E content of plants through metabolic engineering. Science 282:2098–2100Google Scholar
  166. Shukla V, Mattoo AK (2009) Potential for engineering horticultural crops with high antioxidant capacity. CAB Rev Perspect Agric Vet Sci 2009:1–22Google Scholar
  167. Skodda S, Muller T (2013) Refractory epileptic seizures due to vitamin B6 deficiency in a patient with Parkinson’s disease under duodopa® therapy. J Neural Transm 120:315–318CrossRefGoogle Scholar
  168. Smirnoff N (2018) Ascorbic acid metabolism and functions: a comparison of plants and mammals. Free Radical Biol Med 122:116–129Google Scholar
  169. Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Biochem Mol Biol 35:291–314CrossRefGoogle Scholar
  170. Stacey MG, Cahoon RE, Nguyen HT, Cui Y, Sato S, Nguyen CT, Batek J et al (2016) Identification of homogentisate dioxygenase as a target for vitamin E biofortification in oilseeds. Plant Physiol 172:1506–1518Google Scholar
  171. Strobbe S, Van Der Straeten D (2018) Toward eradication of B-vitamin deficiencies: considerations for crop biofortification. Front Plant Sci 9:443CrossRefPubMedPubMedCentralGoogle Scholar
  172. Strobbe S, De Lepeleire J, Van Der Straeten D (2018) From in planta function to vitamin rich food crops: the ACE of biofortification. Front Plant Sci 9Google Scholar
  173. Tambasco-Studart M, Titiz O, Raschle T, Forster G, Amrhein N, Fitzpatrick TB (2005) Vitamin B6 biosynthesis in higher plants. Proc Natl Acad Sci USA 102:13687–13692CrossRefGoogle Scholar
  174. Tanaka T, Tateno Y, Gojobori T (2005) Evolution of vitamin B6 (pyridoxine) metabolism by gain and loss of genes. Mol Biol Evol 22:243–250CrossRefGoogle Scholar
  175. Tang Y, Fu X, Shen Q, Tang K (2016) Roles of MPBQ-MT in promoting alpha/gamma-tocopherol production and photosynthesis under high light in lettuce. PLoS ONE 11:e0148490. Scholar
  176. Tóth SZ, Nagy V, Puthur JT, Kovács L, Garab G (2011) The physiological role of ascorbate as photosystem II electron donor: protection against photoinactivation in heat-stressed leaves. Plant Physiol 156:382–392Google Scholar
  177. Troesch B, Hoeft B, McBurney M, Eggersdorfer M, Weber P (2012) Dietary surveys indicate vitamin intakes below recommendations are common in representative Western countries. British J Nutr 108:692–698Google Scholar
  178. Truffault V, Fry SC, Stevens RG, Gautier H (2017) Ascorbate degradation in tomato leads to accumulation of oxalate, threonate and oxalyl threonate. Plant J 89:996–1008CrossRefGoogle Scholar
  179. Ueland PM, McCann A, Midttun Ø, Ulvik A (2017) Inflammation, vitamin B6 and related pathways. Mol Aspects Med 53:10–27CrossRefGoogle Scholar
  180. Ulatowski LM, Manor D (2015) Vitamin E and neurodegeneration. Neurobiol Dis 84:78–83CrossRefGoogle Scholar
  181. Upadhyaya CP, Young KE, Akula N, Soon Kim H, Heung JJ, Oh OM, Aswath CR, Chun SC, Kim DH et al (2009) Over-expression of strawberry D-galacturonic acid reductase in potato leads to accumulation of vitamin C with enhanced abiotic stress tolerance. Plant Sci 177:659–667CrossRefGoogle Scholar
  182. Ushimaru T, Nakagawa T, Fujioka Y, Daicho K, Naito M, Yamauchi Y, Nonaka H, Amako K, Yamawaki K, Murata N (2006) Transgenic Arabidopsis plants expressing the rice dehydroascorbate reductase gene are resistant to salt stress. J Plant Physiol 163:1179–1184CrossRefGoogle Scholar
  183. Velandia B, Centor RM, McConnell V, Shah M (2008) Scurvy is still present in developed countries. J Gen Intern Med 23:1281–1284Google Scholar
  184. Valpuesta V, Botella MA (2004) Biosynthesis of L-ascorbic acid in plants: new pathways for an old antioxidant. Trends Plant Sci 9:573–577CrossRefGoogle Scholar
  185. Van Eenennaam AL, Lincoln K, Durrett TP, Valentin HE, Shewmaker CK, Thorne GM, Hao M et al (2003) Engineering vitamin E content: from Arabidopsis mutant to soy oil. Plant Cell 15:3007–3019Google Scholar
  186. Vandamme EJ, Revuelta JL (2016) Industrial Biotechnology of vitamins, biopigments and antioxidants.Wiley‐VCH, Weinheim, Germany, p 560Google Scholar
  187. Vanderschuren H, Boycheva S, Li KT, Szydlowski N, Gruissem W, Fitzpatrick TB (2013) Strategies for vitamin B6 biofortification of plants: a dual role as a micronutrient and a stress protectant. Front Plant Sci 4:143CrossRefPubMedPubMedCentralGoogle Scholar
  188. Villanueva C, Kross RD (2012) Antioxidant-induced stress. Int J Mol Sci 13:2091–2109CrossRefPubMedPubMedCentralGoogle Scholar
  189. Vissers MC, Bozonet SM, Pearson JF, Braithwaite LJ (2011) Dietary ascorbate intake affects steady state tissue concentrations in vitamin C-deficient mice: tissue deficiency after sub-optimal intake and superior bioavailability from a food source (kiwifruit). Am J Clin Nutr 93:292–301CrossRefGoogle Scholar
  190. Vogel G (2012) Tropical diseases: mystery disease haunts region. Science 336:144–146CrossRefGoogle Scholar
  191. Wadman M (2011) African outbreak stumps experts. Nature 475:148–149CrossRefGoogle Scholar
  192. Wang Z, Xiao Y, Chen W, Tang K, Zhang L (2010) Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis. J Integr Plant Biol 52:400–409CrossRefGoogle Scholar
  193. Wang J, Yu Y, Zhang Z, Quan R, Zhang H, Ma L, Deng XW et al (2013) Arabidopsis CSN5B interacts with VTC1 and modulates ascorbic acid synthesis. Plant Cell 25:625–636CrossRefPubMedPubMedCentralGoogle Scholar
  194. Wang H, Xu S, Fan Y, Liu N, Zhan W, Liu H, Deng M (2018) Beyond pathways: genetic dissection of tocopherol content in maize kernels by combining linkage and association analyses. Plant Biotechnol J 16:1464–1475Google Scholar
  195. Wevar-Oller AL, Agostini E, Milrad SR, Medina MI (2009) In situ and de novo biosynthesis of vitamin C in wild type and transgenic tomato hairy roots: a precursor feeding study. Plant Sci 177:28–34CrossRefGoogle Scholar
  196. Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369CrossRefGoogle Scholar
  197. Wheeler GL, Ishikawa T, Pornsaksit V, Smirnoff N (2015) Evolution of alternative biosynthetic pathways for vitamin C following plastid acquisition in photosynthetic eukaryotes. eLife 4:e06369.
  198. Wolucka BA, Van Montagu M (2003) GDP-mannose 3′,5′-epimerase forms GDP-L-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants. J Biol Chem 278:47483–47490CrossRefGoogle Scholar
  199. Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C et al (2012) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59–66CrossRefGoogle Scholar
  200. Yabuta Y, Tanaka H, Yoshimura S, Suzuki A, Tamoi M, Maruta T et al (2013) Improvement of vitamin E quality and quantity in tobacco and lettuce by chloroplast genetic engineering. Transgenic Res 22:391–402Google Scholar
  201. Yamamoto A, Bhuiyan MNH, Waditee R, Tanaka Y, Esaka M, Oba K, Jagendorf AT, Takabe T (2005) Suppressed expression of the apoplastic ascorbate oxidase gene increases salt tolerance in tobacco and Arabidopsis plants. J Exp Bot 56:1785–1796CrossRefGoogle Scholar
  202. Yang W, Cahoon RE, Hunter SC, Zhang C, Han J, Borgschulte T, Cahoon EB (2011a) Vitamin E biosynthesis: functional characterization of the monocot homogentisate geranylgeranyl transferase. Plant J 65:206–217Google Scholar
  203. Yang W, Cahoon RE, Hunter SC, Zhang C, Han J, Borgschulte T, Cahoon EB (2011b) Vitamin E biosynthesis: functional characterization of the monocot homogentisate geranylgeranyl transferase. Plant J 65:206–217CrossRefGoogle Scholar
  204. Yin L, Wang S, Eltayeb AE, Uddin MI, Yamamoto Y, Tsuji W et al (2010) Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231:609–621CrossRefGoogle Scholar
  205. Zhang W, Gruszewski HA, Chevone BI, Nessler CL (2008) An Arabidopsis purple acid phosphatase with phytase activity increases foliar ascorbate. Plant Physiol 146:431–440CrossRefPubMedPubMedCentralGoogle Scholar
  206. Zhang W, Lorence A, Gruszewski HA, Chevone BI, Nessler CL (2009) AMR1, an Arabidopsis gene that coordinately and negatively regulates the mannose/L-galactose ascorbic acid biosynthetic pathway. Plant Physiol 150:942–950CrossRefPubMedPubMedCentralGoogle Scholar
  207. Zhang C, Liu J, Zhang Y, Cai X, Gong P, Zhang J et al (2010) Overexpression of SlGMEs leads to ascorbate accumulation with enhanced oxidative stress, cold, and salt tolerance in tomato. Plant Cell Rep 30:389–398CrossRefGoogle Scholar
  208. Zhang Z, Wang J, Zhang R, Huang R (2012) The ethylene response factor AtERF98 enhances tolerance to salt through the transcriptional activation of ascorbic acid synthesis in Arabidopsis. Plant J 71:273–287CrossRefGoogle Scholar
  209. Zhang GY, Liu RR, Xu G, Zhang P, Li Y, Tang KX et al (2013) Increased alpha-tocotrienol content in seeds of transgenic rice overexpressing Arabidopsis gamma-tocopherol methyltransferase. Transgenic Res 22:89–99CrossRefGoogle Scholar
  210. Zhang W, Liu T, Ren G, Hörtensteiner S, Zhou Y, Cahoon EB, Zhang C (2014) Chlorophyll degradation: the tocopherol biosynthesis related phytol hydrolase in Arabidopsis seeds is still missing. Plant Physiol 166:70–79Google Scholar
  211. Zhang GY, Liu RR, Zhang CQ, Tang KX, Sun MF, Yan GH, Liu QQ (2015a) Manipulation of the rice L-galactose pathway: evaluation of the effects of transgene overexpression on ascorbate accumulation and abiotic stress tolerance. PLoS ONE 10:e0125870CrossRefPubMedPubMedCentralGoogle Scholar
  212. Zhang C, Zhang W, Ren G, Li D, Rebecca EC, Chen M, Cahoon E (2015b) Chlorophyll synthase under epigenetic surveillance is critical for vitamin E tocopherol synthesis and altered expression impacts tocopherol levels in Arabidopsis. Plant Physiol 168:1503–1511Google Scholar
  213. Zhang H, Si X, Ji X, Fan R, Liu J, Chen K, Gao C (2018) Genome editing of upstream open reading frames enables translational control in plants. Nat BiotechnolGoogle Scholar
  214. Zhou Y, Tao QC, Wang ZN, Fan R, Li Y, Sun XF, Tang KX (2012) Engineering ascorbic acid biosynthetic pathway in Arabidopsis leaves by single and double gene transformation. Biol Plant 56:451–457CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Manish Sainger
    • 1
  • Darshna Chaudhary
    • 2
  • Ranjana Jaiwal
    • 3
  • Anil K. Chhillar
    • 2
  • Pawan Kumar Jaiwal
    • 2
    Email author
  1. 1.Department of BiotechnologyU. I. E. T, Maharshi Dayanand UniversityRohtakIndia
  2. 2.Centre for BiotechnologyMaharshi Dayanand UniversityRohtakIndia
  3. 3.Department of ZoologyMaharshi Dayanand UniversityRohtakIndia

Personalised recommendations