Abstract
The fruit of Actinidia are unusual in that they contain very high concentrations of vitamin C—over 80 mg/100 g fresh weight (FW) in commercial cultivars and over 800 mg/100 g FW in some wild species. In this review, we describe the genes for various proposed pathways for ascorbate production, via l-galactose, via glucuronate from myo-inositol and via galacturonate from pectin. We then focus on the l-galactose pathway genes and enzymes identified in kiwifruit. We also discuss the presence of genes that recycle ascorbate and the production of oxalate, another metabolite with a high concentration in kiwifruit. Lastly, we discuss two levels of regulation of ascorbate biosynthesis in kiwifruit, at the transcriptional level through the gene that encodes the enzyme GDP-galactose phosphorylase (GGP) and at the translational level through feedback control of GGP translation involving a upstream open reading frame on the 5′ untranslated region of GGP.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Agius F, González-Lamothe R, Caballero JL, Muñoz-Blanco J, Botella MA, Valpuesta V (2003) Engineering increased vitamin C levels in plants by overexpression of a d-galacturonic acid reductase. Nat Biotechnol 21:177–181
Alhagdow M, Mounet F, Gilbert L, Nunes-Nesi A, Garcia V, Just D et al (2007) Silencing of the mitochondrial ascorbate synthesizing enzyme l-galactono-1,4-lactone dehydrogenase affects plant and fruit development in tomato. Plant Physiol 145:1408–1422
Amaya I, Osorio S, Martinez-Ferri E, Lima-Silva V, Doblas VG, Fernández-Muñoz R et al (2014) Increased antioxidant capacity in tomato by ectopic expression of the strawberry d-galacturonate reductase gene. Biotechnol J 10:490–500
Badejo AA, Tanaka N, Esaka M (2007) Analysis of GDP-d-mannose pyrophosphorylase gene promoter from acerola (Malpighia glabra) and increase in ascorbate content of transgenic tobacco expressing acerola gene. Plant Cell Physiol 49:126–132
Badejo AA, Eltelib HA, Fukunaga K, Fujikawa Y, Esaka M (2009) Increase in ascorbate content of transgenic tobacco plants overexpressing the acerola (Malpighia glabra) phosphomannomutase gene. Plant Cell Physiol 50:423–428
Badejo AA, Wada K, Gao YS, Maruta T, Sawa Y, Shigeoka S, Ishikawa T (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 63:229–239
Bieleski RL, Clark CJ, Klages KU (1997) Identification of myo-inositol as a major carbohydrate in kiwifruit, Actinidia deliciosa. Phytochemistry 46:51–55
Bulley SM, Rassam M, Hoser D, Otto W, Schünemann N, Wright M et al (2009) 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. J Exp Bot 60(3):765–778
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 10:390–397
Chen Z, Young TE, Ling J, Chang S-C, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Nat Acad Sci USA 100:3525–3530
Cheng CH, Seal AG, Boldingh HL, Marsh KB, MacRae EA, Murphy SJ et al (2004) Inheritance of taste characters and fruit size and number in a diploid Actinidia chinensis (kiwifruit) population. Euphytica 138:185–195
Chesoniene L, Daubaras R, Viskelis P (2004) Biochemical composition of berries of some Kolomikta kiwi (Actinidia kolomikta) cultivars and detection of harvest maturity. Acta Hort 663:305–308
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 281:15662–15670
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 64:2793–2804
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 235:553–564
Crowhurst RN, Gleave AP, MacRae EA, Ampomah-Dwamena C, Atkinson RG, Beuning LL et al (2008) Analysis of expressed sequence tags from Actinidia: applications of a cross species EST database for gene discovery in the areas of flavor, health, color and ripening. BMC Genom 9:351
Di Matteo A, Sacco A, Anacleria M, Pezzotti M, Delledonne M, Ferrarini A et al (2010) The ascorbic acid content of tomato fruits is associated with the expression of genes involved in pectin degradation. BMC Plant Biol 10:163
Dowdle J, Ishikawa T, Gatzek S, Rolinski S, Smirnoff N (2007) Two genes in Arabidopsis thaliana encoding GDP-l-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. Plant J 52:673–689
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 127:57–65
Ferguson AR (1991) Kiwifruit (Actinidia). Acta Hort 290:603–656
Ferguson AR, Ferguson LR (2003) Are kiwifruit really good for you? Acta Hort 610:131–138
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18
Fraser LG, Tsang GK, Datson PM, De Silva HN, Harvey CF, Gill GP et al (2009) A gene-rich linkage map in the dioecious species Actinidia chinensis (kiwifruit) reveals putative X/Y sex-determining chromosomes. BMC Genom 10:102
Gao Y, Badejo AA, Shibata H, Sawa Y, Maruta T, Shigeoka S et al (2011) Expression analysis of the VTC2 and VTC5 genes encoding GDP-l-galactose phosphorylase, an enzyme involved in ascorbate biosynthesis, in Arabidopsis thaliana. Biosci Biotechnol Biochem 75:1783–1788
Gatzek S, Wheeler GL, Smirnoff N (2002) 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 30:541–553
Gest N, Garchery C, Gautier H, Jiménez A, Stevens R (2012) Light-dependent regulation of ascorbate in tomato by a monodehydroascorbate reductase localized in peroxisomes and the cytosol. Plant Biotechnol J 11:344–354
Gilbert L, Alhagdow M, Nunes-Nesi A, Quemener B, Guillon F, Bouchet B et al (2009) GDP-d-mannose 3,5-epimerase (GME) plays a key role at the intersection of ascorbate and non-cellulosic cell-wall biosynthesis in tomato. Plant J 60:499–508
Gillaspy GE, Keddie JS, Oda K, Gruissem W (1995) Plant inositol monophosphatase is a lithium-sensitive enzyme encoded by a multigene family. Plant Cell 7:2175–2185
Goo Y-M, Chun H, Kim T-W, Lee C-H, Ahn M-J, Bae S-C et al (2008) Expressional characterization of dehydroascorbate reductase cDNA in transgenic potato plants. J Plant Biol 51:35–41
Green MA, Fry SC (2005) Vitamin C degradation in plant cells via enzymatic hydrolysis of 4-O-oxalyl-l-threonate. Nature 433:83–87
Gu X, Bar-Peled M (2004) The biosynthesis of UDP-galacturonic acid in plants. Functional cloning and characterization of Arabidopsis UDP-d-glucuronic acid 4-epimerase. Plant Physiol 136:4256–4264
Handford MG, Baldwin TC, Goubet F, Prime TA, Miles J, Yu X et al (2003) Localisation and characterisation of cell wall mannan polysaccharides in Arabidopsis thaliana. Planta 218:27–36
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 49:1244–1249
Hemavathi, Upadhyaya CP, Young KE, Akula N, soon Kim H 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 177:659–667
Huang H-W, Ferguson AR (2007) [incorrectly published as Ferguson AR, Huang H-W] Genetic resources of kiwifruit: Domestication and breeding. Hort Rev 33: 1-121
Huang H-W, Wang Y, Zhang Z-H, Jiang Z-W, Wang S-M (2004) Actinidia germplasm resources and kiwifruit industry In China. HortScience 39:1165–1172
Huang S, Ding J, Deng D, Tang W, Sun H, Liu D et al (2013) Draft genome of the kiwifruit Actinidia chinensis. Nat Commun 4:2640
Huang M, Xu Q, Deng X-X (2014) l-Ascorbic acid metabolism during fruit development in an ascorbate-rich fruit crop chestnut rose (Rosa roxburghii Tratt). J Plant Physiol 171:1205–1216
Imai T, Niwa M, Ban Y, Hirai M, Ôba K, Moriguchi T (2009) Importance of the l-galactonolactone pool for enhancing the ascorbate content revealed by l-galactonolactone dehydrogenase overexpressing tobacco plants. Plant Cell Tiss Org Cult 96:105–112
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 Tiss Organ Cult 111:1–13
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 60:663–678
Kavitha K, George S, Venkataraman G, Parida A (2010) A salt-inducible chloroplastic monodehydroascorbate reductase from halophyte Avicennia marina confers salt stress tolerance on transgenic plants. Biochimie 92:1321–1329
Keates SE, Tarlyn NM, Loewus FA, Franceschi VR (2000) l-Ascorbic acid and l-galactose are sources for oxalic acid and calcium oxalate in Pistia stratiotes. Phytochemistry 53:433–440
Keller R, Springer F, Renz FS, Kossmann J (1999) Antisense inhibition of the GDP-mannose pyrophosphorylase reduces the ascorbate content in transgenic plants leading to developmental changes during senescence. Plant J 19:131–141
Klages K, Donnison H, Boldingh H, MacRae E (1998) myo-Inositol is the major sugar in Actinidia arguta during early fruit development. Aust J Plant Physiol 25:61–67
Kostman TA, Tarlyn NM, Loewus FA, Franceschi VR (2001) Biosynthesis of l-ascorbic acid and conversion of carbons 1 and 2 of l-ascorbic acid to oxalic acid occurs within individual calcium oxalate crystal idioblasts. Plant Physiol 125:634–640
Kwon S-Y, Choi S-M, Ahn Y-O, Lee H-S, Lee H-B, Park Y-M et al (2003) Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbate reductase gene. J Plant Physiol 160:347–353
Laing WA, Frearson N, Bulley S, MacRae, E (2004a) Kiwifruit l-galactose dehydrogenase; molecular, biochemical and physiological aspects of the enzyme. Funct Plant Biol 31:1015–1025
Laing WA, Bulley S, Wright M, Cooney J, Jensen D, Barraclough D, MacRae E (2004) A highly specific l-galactose-1-phosphate phosphatase on the path to ascorbate biosynthesis. Proc Natl Acad Sci USA 101:16976–16981
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 Natl Acad Sci USA 104:9534–9539
Laing WA, Martínez-Sánchez 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 27:772–786
Li F, Wu Q-Y, Sun Y-L, Wang L-Y, Yang X-H, Meng Q-W (2010a) Overexpression of chloroplastic monodehydroascorbate reductase enhanced tolerance to temperature and methyl viologen-mediated oxidative stresses. Physiol Plant 139:421–434
Li M-J, Ma F-W, Liang D, Li J, Wang Y-L (2010b) Ascorbate biosynthesis during early fruit development is the main reason for its accumulation in kiwi. PLoS ONE 5:e14281
Li M-J, Liu J, Liang D, Guo C-M, Ma F-W (2011) The relationship between GalUR expression and ascorbate accumulation in kiwifruit. Acta Hort Sin 38:1641–1649
Li J, Liang D, Li M, Ma F (2013a) Light and abiotic stresses regulate the expression of GDP-l-galactose phosphorylase and levels of ascorbic acid in two kiwifruit genotypes via light-responsive and stress-inducible cis-elements in their promoters. Planta 238:535–547
Li J, Li M, Liang D, Cui M, Ma F (2013b) Expression patterns and promoter characteristics of the gene encoding Actinidia deliciosa l-galactose-1-phosphate phosphatase involved in the response to light and abiotic stresses. Mol Biol Rep 40:1473–1485
Li J, Cui M, Li M, Wang X, Liang D, Ma F (2013c) Expression pattern and promoter analysis of the gene encoding GDP-d-mannose 3′,5′-epimerase under abiotic stresses and applications of hormones by kiwifruit. Scientia Hort 150:187–194
Li J, Li M, Liang D, Ma F, Lei Y (2014) Comparison of expression pattern, genomic structure, and promoter analysis of the gene encoding GDP-l-galactose phosphorylase from two Actinidia species. Scientia Hort 169:206–213
Linster CL, Clarke SG (2008) l-Ascorbate biosynthesis in higher plants: the role of VTC2. Trends Plant Sci 13:567–573
Linster CL, Adler LN, Webb K, Christensen KC, Brenner C, Clarke SG (2008) A second GDP-l-galactose phosphorylase in Arabidopsis en route to vitamin C: Covalent intermediate and substrate requirements for the conserved reaction. J Biol Chem 283:18483–18492
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 36:2331–2341
Marsh KB, Boldingh HL, Shilton RS, Laing WA (2009) Changes in quinic acid metabolism during fruit development in three kiwifruit species. Funct Plant Biol 36:463–470
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 283:28842–28851
Massot C, Stevens R, Génard M, Longuenesse J-J, Gautier H (2012) Light affects ascorbate content and ascorbate-related gene expression in tomato leaves more than in fruits. Planta 235:153–163
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 160:1613–1629
Miyaji T, Kuromori T, Takeuchi Y, Yamaji N, Yokosho K, Shimazawa A et al (2015) AtPHT4;4 is a chloroplast-localized ascorbate transporter in Arabidopsis. Nat Commun 6:5928
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 106:7762–7767
Qian W, Yu C, Qin H, Liu X, Zhang A, Johansen IE, Wang D (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 49:399–413
Qin A, Shi Q, Yu X (2011) Ascorbic acid contents in transgenic potato plants overexpressing two dehydroascorbate reductase genes. Mol Biol Rep 38:1557–1566
Rassam M, Laing W (2005) Variation in ascorbic acid and oxalate levels in the fruit of Actinidia chinensis tissues and genotypes. J Agric Food Chem 53:2322–2326
Rassam M, Bulley SM, Laing WA (2007) Oxalate and ascorbate in Actinidia fruit and leaves. Acta Hort 753:479–484
Richardson AC, Marsh KB, Boldingh HL, Pickering AH, Bulley SM, Frearson NJ et al (2004) High growing temperatures reduce fruit carbohydrate and vitamin C in kiwifruit. Plant Cell Environ 27:423–435
Tabata K, Oba K, Suzuki K, Esaka M (2001) Generation and properties of ascorbic acid-deficient transgenic tobacco cells expressing antisense RNA for l-galactono-1,4- actone dehydrogenase. Plant J 27:139–148
Torabinejad J, Donahue JL, Gunesekera BN, Allen-Daniels MJ, Gillaspy GE (2009) VTC4 is a bifunctional enzyme that affects myoinositol and ascorbate biosynthesis in plants. Plant Physiol 150:951–961
Usadel B, Schlüter U, Mølhøj M, Gipmans M, Verma R, Kossmann J, Reiter W-D et al (2004) Identification and characterization of a UDP-glucuronate 4-epimerase in Arabidopsis. FEBS Lett 569:327–331
Wang Z-Y, MacRae EA, Wright MA, Bolitho KM, Ross GS, Atkinson RG (2000) Polygalacturonase gene expression in kiwifruit: relationship to fruit softening and ethylene production. Plant Mol Biol 42:317–328
Wang H-S, Yu C, Zhu Z-J, Yu X-C (2011) Overexpression in tobacco of a tomato GMPase gene improves tolerance to both low and high temperature stress by enhancing antioxidation capacity. Plant Cell Rep 30:1029–1040
Wang J, Zhang Z, Huang R (2013a) Regulation of ascorbic acid synthesis in plants. Plant Signaling Behavior 8:e24536
Wang J, Yu Y, Zhang Z, Quan R, Zhang H, Ma L et al (2013b) Arabidopsis CSN5B interacts with VTC1 and modulates ascorbic acid synthesis. Plant Cell Online 25:625–636
Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369
Wheeler G, Ishikawa T, Pornsaksit V, Smirnoff N (2015) Evolution of alternative biosynthetic pathways for vitamin C following plastid acquisition in photosynthetic eukaryotes. eLife 4:e06369
Yabuta Y, Mieda T, Rapolu M, Nakamura A, Motoki T, Maruta T et al (2007) Light regulation of ascorbate biosynthesis is dependent on the photosynthetic electron transport chain but independent of sugars in Arabidopsis. J Exp Bot 58:2661–2671
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 231:609–621
Zablackis E, York WS, Pauly M, Hantus S, Reiter WD, Chapple CC et al (1996) Substitution of l-fucose by l-galactose in cell walls of Arabidopsis mur1. Science 272:1808–1810
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 150:942–950
Zhang C, Liu J, Zhang Y, Cai X, Gong P, Zhang J et al (2011) Overexpression of SlGMEs leads to ascorbate accumulation with enhanced oxidative stress, cold, and salt tolerance in tomato. Plant Cell Rep 30:389–398
Zhang Z, Wang J, Zhang R, Huang R (2012) The ethylene response factor ERF protein AtERF98 enhances tolerance to salt through the transcriptional activation of ascorbic acid synthesis in Arabidopsis. Plant J 71:273–287
Zhang G-Y, Liu R-R, Zhang C-Q, Tang K-X, Sun M-F, Yan G-H, Liu Q-Q (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:e0125870
Zhang L, Ma G, Yamawaki K, Ikoma Y, Matsumoto H, Yoshioka T et al (2015b) Regulation of ascorbic acid metabolism by blue LED light irradiation in citrus juice sacs. Plant Sci 233:134–142
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 56:451–457
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Bulley, S.M., Laing, W. (2016). Ascorbic Acid-Related Genes. In: Testolin, R., Huang, HW., Ferguson, A. (eds) The Kiwifruit Genome. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-319-32274-2_13
Download citation
DOI: https://doi.org/10.1007/978-3-319-32274-2_13
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-32272-8
Online ISBN: 978-3-319-32274-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)