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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

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Abstract

Ascorbic acid (AA) is one of the most powerful natural antioxidant able to prevent enzymatic browning after exogenous treatment of minimally-processed products. The specific mechanism by which AA prevents enzymatic browning remains still debated and a direct effect of endogenous AA stimulation and browning has never been studied. The manipulation of AA pathway is a promising approach to study the biochemical mechanism by which AA acts as an anti-browning agent. In this work, cDNA of L-galactono-1,4-lactone dehydrogenase (L-GalLDH), one of the key gene of the Smirnoff–Wheeler’s branch of AA biosynthetic pathway, was isolated and overexpressed in lettuce (Lactuca sativa L. cv ‘Iceberg’), a species highly prone to browning. The hypothesis that the overexpression of L-GalLDH translates to AA accumulation and reduces the browning phenomena in lettuce leaves after cutting was tested. Our results indicate that transgenic lettuce plants, showing about 19-fold overexpression of L-GalLDH as compared to wild type, had about +30 % of AA concentration in mature leaves. Transgenic plants exhibited reduced browning over the leaves, even 10 day after cutting, as demonstrated by higher values of luminosity (L*) and higher values of greenness (a*) compared to control plants. Overall, these findings provide a first evidence of the role of endogenous AA as browning-preventing agent. The obtainment of T2 transgenic lettuce plants is a promising first step to further determine the specific mechanism by which AA acts as an anti-browning preservative.

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Abbreviations

AA :

L-Ascorbic acid (sum of reduced and oxidized form of ascorbic acid)

ALO:

D-Arabinono-γ-lactone oxidase

AsA:

Reduced form of ascorbic acid

BAP:

6-Benzylaminopurine

DHA:

Dehydroascorbate

DTT:

Dithiothreitol

ESTs:

Expressed sequence tags

GDP:

Guanosine diphosphate

GGT:

GDP-L-galactose guanyltransferase

L-GalLDH:

L-galactono-1,4-lactone dehydrogenase

GLO:

L-gulono-1,4-lactone oxidase

GUO:

D-gluconolactone oxidase

LsL-GalLDH:

Lactuca sativa L-galactono-1,4-lactone dehydrogenase

MS:

Murashige and Skoog medium

NAA:

α-Naphthalene-acetic-acid

POXs:

Peroxidases

PPOs:

Polyphenol oxidases

RACE:

Rapid amplification of cDNA ends

References

  • Alhagdow M, Mounet F, Gilbert L, Nunes-Nesi A, Garcia V, Just D, Petit J, Beauvoit B, Fernie AR, Rothan C, Baldet P (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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationship in green cells. Physiol Plant 100:224–233

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Altunkaya A, Gökmen V (2009) Effect of anti-browning agents on phenolic compounds profile of fresh lettuce (L. sativa). Food Chem 117:122–126

    Article  CAS  Google Scholar 

  • Badejo AA, Eltelib HA, Fukunaga K, Fujikawa Y, Esaka M (2009) Increase in ascorbate content of transgenic plants overexpressing the acerola (Malpighia glabra) phosphomannomutase gene. Plant Cell Physiol 50:423–428

    Article  CAS  PubMed  Google Scholar 

  • Bartoli CG, Pastori GM, Foyer CH (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes III and IV. Plant Physiol 123:335–343

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bartoli CG, Guiamet JJ, Kiddle G, Pastori GM, Di Cagno R, Theodoulou FL, Foyer CH (2005) Ascorbate content of wheat leaves is not determined by maximal L-galactono-1,4-lactone dehydrogenase (GalLDH) activity under drought stress. Plant Cell Environ 28:1073–1081

    Article  CAS  Google Scholar 

  • Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer ELL (2002) The pfam protein families database. Nucleic Acids Res 30:276–280

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bottino A, Degl’Innocenti E, Guidi L, Graziani G, Fogliano V (2009) Bioactive compounds during storage of fresh-cut spinach: the role of endogenous ascorbic acid in the improvement of produce quality. J Agric Food Chem 57:2925–2931

    Article  CAS  PubMed  Google Scholar 

  • Brown NJ, Sullivan JA, Gray JC (2005) Light and plastid signals regulate the expression of the pea plastocyanin gene through a common region at the 5′ end of the coding region. Plant J 4:541–552

    Article  Google Scholar 

  • Bulley S, Wright M, Rommens C, Yan H, Rassam M, Lin-Wang K, Andre C, Brewster D, Karunairetnam S, Allan AC, Laing WA (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

    Article  CAS  PubMed  Google Scholar 

  • Castañer M, Gil MI, Ruiz MV, Artes F (1999) Browning susceptibility of minimally processed Baby and Romaine lettuces. Eur Food Res Technol 209:52–56

    Article  Google Scholar 

  • Claros MG, Vincens P (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 241:779–786

    Article  CAS  PubMed  Google Scholar 

  • Cocetta G, Karppinen K, Suokas M, Hohtola A, Häggman H, Spinardi A, Mignani I, Jaakola L (2012) Ascorbic acid metabolism during bilberry (Vaccinium myrtillus L.) fruit development. J Plant Physiol 169:1059–1065

    Article  CAS  PubMed  Google Scholar 

  • Cruz-Rus E, Amaya I, Valpuesta V (2012) The challenge of increasing vitamin C content in plant foods. Biotechnol J 7:1110–1121

    Article  CAS  PubMed  Google Scholar 

  • Curtis IS, Power JB, Blackhall NW, de Laat AMM, Davey MR (1994) Genotype-independent transformation of lettuce using Agrobacterium tumefaciens. J Exp Bot 45:1441–1449

    Article  CAS  Google Scholar 

  • Degl’Innocenti E, Pardossi A, Tognoni F, Guidi L (2007) Physiological basis of sensitivity to enzymatic browning in ‘lettuce’, ‘escarole’ and ‘rocket salad’ when stored as fresh-cut products. Food Chem 104:209–215

    Article  Google Scholar 

  • Dowdle J, Ishikawa T, Gatzek S, Rolinski S, Smirnoff N (2007) Two genes in Arabidopsis thaliana encoding GDPp-L-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. Plant J 52:673–689

    Article  CAS  PubMed  Google Scholar 

  • Falquet L, Pagni M, Bucher P, Hulo N, Sigrist CJ, Hofmann K, Bairoch A (2002) The PROSITE database, its status in 2002. Nucleic Acids Res 30:235–238

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fraaije MW, Van Berkel WJH, Benen JAE, Visser J, Mattevi A (1998) A novel oxidoreductase family sharing a conserved FAD-binding domain. Trends Biochem Sci 23:206–207

    Article  CAS  PubMed  Google Scholar 

  • Fraaije MW, van den Heuvel RHH, van Berkel WJH, Mattevi A (2000) Structural analysis of flavinylation in vanillyl-alcohol oxidase. J Biol Chem 275:38654–38658

    Article  CAS  PubMed  Google Scholar 

  • Frugis G, Giannino D, Mele G, Nicolodi C, Chiappetta A, Bitonti MB, Innocenti AM, Dewitte W, Van Onckelen H, Mariotti D (2001) Overexpression of KNAT1 in lettuce shifts leaf determinate growth to a shoot-like indeterminate growth associated with an accumulation of isopentenyl-type cytokinins. Plant Physiol 126:1370–1380

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gallie DR (2013) The role of L-ascorbic acid recycling in responding to environmental stress and promoting plant growth. J Exp Bot 64:433–443

    Article  CAS  PubMed  Google Scholar 

  • Gerszberg A, Hnatuszko-Konka K, Kowalczyk T, Kononowicz AK (2015) Tomato (Solanum lycopersicum L.) in the service of biotechnology. Plant Cell Tiss Organ Cult 120:881–902

    Article  CAS  Google Scholar 

  • Guo X, Liu RH, Fu X, Sun X, Tang K (2013) Over-expression of L-galactono-γ-lactone dehydrogenase increases vitamin C, total phenolics and antioxidant activity in lettuce through bio-fortification. Plant Cell Tiss Organ Cult 114:225–236

    Article  CAS  Google Scholar 

  • Hancock RD, Viola R (2002) Biotechnological approaches for L-ascorbic acid production. Trends Biotechnol 20:299–305

    Article  CAS  PubMed  Google Scholar 

  • Hancock RD, Viola R (2005) Improving the nutritional value of crops through enhancement of L-ascorbic acid (vitamin C) content: rationale and biotechnological opportunity. J Agric Food Chem 58:5248–5257

    Article  Google Scholar 

  • Hemavathi-Upadhyaya CP, Akula N, Young KE, Chun SC, Kim DH, Park SW (2010) Enhanced ascorbic acid accumulation in transgenic potato confers tolerance to various abiotic stresses. Biotechnol Lett 32:321–330

    Article  Google Scholar 

  • Imai T, Ban Y, Terakami S, Yamamoto T, Moriguchi T (2009) L-Ascorbate biosynthesis in peach: cloning of six L-galactose pathway-related genes and their expression during peach fruit development. Physiol Plant 136:139–149

    Article  CAS  PubMed  Google Scholar 

  • Ioannidi E, Kalamaki MS, Engineer C, Pateraki I, Alexandrou D, Mellidou I, Giovannonni J, Kanellis AK (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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ishikawa T, Dowdle J, Smirnoff N (2006) Progress in manipulating ascorbic acid biosynthesis and accumulation in plants. Physiol Plant 126:343–355

    Article  CAS  Google Scholar 

  • Kaewubon P, Hutadilok-Towatana N, Teixeira da Silva J, Meesawat U (2015) Ultrastructural and biochemical alterations during browning of pigeon orchid (Dendrobium crumenatum Swartz) callus. Plant Cell Tiss Organ Cult 121:53–69

    Article  CAS  Google Scholar 

  • Kampfenkel K, Van Montagu M, Inzé D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem 225:165–167

    Article  CAS  PubMed  Google Scholar 

  • Ke D, Saltveit ME (1989) Wound induced ethylene production, phenolic metabolism and susceptibility to russet spotting in Iceberg lettuce. Physiol Plant 76:412–418

    Article  CAS  Google Scholar 

  • King AD, Magnuson JA, Torok T, Godman N (1991) Microflora and storage quality of partially processed lettuce. J Food Sci 56:459–461

    Article  Google Scholar 

  • Laing W, Wright M, Cooney J, Bulley S (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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Landi M, Degl’Innocenti E, Guglielminetti L, Guidi L (2013) Role of ascorbic acid in polyphenol-oxidase inhibition and browning prevention in different browning-sensitive Lactuca sativa var. capitata (L.) and Eruca sativa (Mill.) stored as fresh-cut products. J Sci Food Agric 93:1814–1819

    Article  CAS  PubMed  Google Scholar 

  • Leferink NGH, van den Berg WAM, van Berkel WJH (2008) L-Galactono-γ-lactone dehydrogenase from Arabidopsis thaliana, a flavoprotein involved in vitamin C biosynthesis. FEBS J 275:713–726

    Article  CAS  PubMed  Google Scholar 

  • Leferink NGH, Mac Donald FJ, van den Berg WAM, van Berkel WJH (2009) Functional assignment of Glu386 and Arg388 in the active site of L-Galactono-γ-lactone dehydrogenase. FEBS Lett 583:3199–3203

    Article  CAS  PubMed  Google Scholar 

  • Li MJ, Ma FW, Guo CM, Liu J (2010) Ascorbic acid formation and profiling of genes expressed in its synthesis and recycling in apple leaves of different ages. Plant Physiol Biochem 48:216–224

    Article  CAS  PubMed  Google Scholar 

  • Li M, Chen X, Wang P, Ma F (2011) Ascorbic acid accumulation and expression of gene involved in its biosynthesis and recycling in developing apple fruit. J Am Soc Hortic Sci 136:231–238

    CAS  Google Scholar 

  • Linster CL, Clarke SG (2008) L-Ascorbate biosynthesis in higher plants: the role of VTC2. Trends Plant Sci 13:567–573

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Linster CL, Adler LN, Webb K, Christensen KC, Brenner C, Clarke SG (2007) 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 282:18482–18492

    Article  Google Scholar 

  • Liu Y, Yu L, Tong J, Ding J, Wang R, Lu Y, Xiao L (2013) Tiller number is altered in the ascorbic acid-deficient rice suppressed for L-galactono-1,4-lactone dehydrogenase. J Plant Physiol 170:389–396

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Loscos M, Matamoros A, Becana M (2008) Ascorbate and homoglutathione metabolism in common bean nodules under stress conditions and during natural senescence. Plant Physiol 146:1282–1292

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martin-Diana AB, Rico D, Barry-Ryan C, Frias JM, Mulcahy J, Henehan GTM (2005) Calcium lactate washing treatments for salad-cut Iceberg lettuce: effect of temperature and concentration on quality retention parameters. Food Res Int 38:729–740

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Ôba K, Fukui M, Imai Y, Iriyama S, Nogami K (1994) L-Galactono-γ-lactone dehydrogenase: partial characterization, induction of activity and role in synthesis of ascorbic acid in wounded white potato tuber tissue. Plant Cell Physiol 35:473–478

    Google Scholar 

  • Ôba K, Ishikawa S, Nishikawa M, Mizuno H, Yamamoto T (1995) Purification and properties of L-galactono-γ-lactone dehydrogenase, a key enzyme for ascorbic acid biosynthesis, from sweet potato roots. J Biochem 117:120–124

    PubMed  Google Scholar 

  • Østergaard J, Persiau G, Davey M, Bauw G, Van Montagu M (1997) Isolation of a cDNA coding for L-galactono-γ-lactone dehydrogenase, an enzyme involved in the biosynthesis of ascorbic acid in plants: purification, characterization, cDNA cloning, and expression in yeast. J Biol Chem 272:30009–30016

    Article  PubMed  Google Scholar 

  • Osuga D, Van der Schaaf A, Whitaker JR (1994) Control of PPO activity using a catalytic mechanism. In: Yada RY, Jackman RL, Smith JL (eds) Protein structure-function relationship in foods. Springer, New York, pp 62–88

    Chapter  Google Scholar 

  • Pateraki I, Sanmartin M, Kalamaki M, Gerasopoulos D, Kanellis AK (2004) Molecular characterization and expression studies during melon fruit development and ripening of L-galactono-1,4-lactone dehydrogenase. J Exp Bot 55:1623–1633

    Article  CAS  PubMed  Google Scholar 

  • Pineau B, Layoune O, Danon A, De Paepe R (2008) L-Galactono-1,4-lactone dehydrogenase is required for the accumulation of plant respiratory complex I. J Biol Chem 283:32500–32505

    Article  CAS  PubMed  Google Scholar 

  • Pwee KH, Gray JC (2008) The pea plastocyanin promoter direct cell-specific but not full light-regulated expression in transgenic plants. Plant J 3:437–449

    Article  Google Scholar 

  • Rai MK, Shekhawat NS (2014) Recent advances in genetic engineering for improvement of fruit crops. Plant Cell Tiss Organ Cult 116:1–15

    Article  CAS  Google Scholar 

  • Ren J, Chen Z, Duan W, Somg X, Liu T, Wang J, Hou X, Li Y (2013) Comparison of ascorbic acid biosynthesis in different tissues of three non-heading Chinese cabbage cultivars. Plant Physiol Biochem 73:229–236

    Article  CAS  PubMed  Google Scholar 

  • Rivera JRE, Stone MB, Stushnoff C, Pilon-Smith E, Kendall PA (2006) Effects of ascorbic acid applied by two hydrocooling methods on physical and chemical properties of green leaf lettuce stored at 5 °C. J Food Sci 71:S270–S276

    Article  Google Scholar 

  • Rosales-Mendoza S, Soria-Guerra RE, Moreno-Fierros L, Alpuche-Solís ÁG, Martínez-Gonzáles L, Korban SS (2010) Expression o fan immunogenic F1-V fusion protein in lettuce as a plant-based vaccine against plague. Planta 232:409–416

    Article  CAS  PubMed  Google Scholar 

  • Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum evolution trees. Mol Biol Evol 9:945–967

    CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Saltveit ME (2000) Wound induced changes in phenolic metabolism and tissue browning are altered by heat shock. Postharvest Biol Technol 21:61–69

    Article  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Schertl P, Sunderhaus S, Klodmann J, Gergoff Grozeff GE, Bartoli CG, Braun H-P (2012) L-Galactono-1,4-lactone dehydrogenase (GLDH) forms a part of three subcomplexes of mitochondrial complex I in Arabidopsis thaliana. J Biol Chem 287:14412–14419

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Siendones E, González-Reyes JA, Santos-Ocaña C, Navas P, Córdoba F (1999) Biosynthesis of ascorbic acid in kidney bean. L-Galactono-γ-lactone dehydrogenase is an intrinsic protein located at the mitochondrial inner membrane. Plant Physiol 120:907–912

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smirnoff N, Conklin PL, Loewus FA (2001) Biosynthesis of ascorbic acid in plants: a renaissance. Annu Rev Plant Physiol Plant Mol Biol 52:437–467

    Article  CAS  PubMed  Google Scholar 

  • Szarka A, Bánhegyi G, Asard H (2013) The inter-relationship of ascorbate transport, metabolism and mitochondrial, plastidic respiration. Antioxid Redox Signal 19:1036–1044

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tabata K, Ôba K, Suzuki K, Esaka M (2001) Generation and properties of ascorbic acid-deficient transgenic tobacco cells expressing antisense RNA for L-galactono-1,4-lactone dehydrogenase. Plant J 27:139–148

    Article  CAS  PubMed  Google Scholar 

  • Tabata K, Takaoka T, Esaka M (2002) Gene expression of ascorbic acid-related enzymes in tobacco. Phytochemistry 61:631–635

    Article  CAS  PubMed  Google Scholar 

  • Tamaoki M, Mukai F, Asai N, Nakajima N, Kubo A, Aono M, Saji H (2003) Light-controlled expression of a gene encoding L-galactono-γ-lactone dehydrogenase which affects ascorbate pool size in Arabidopsis thaliana. Plant Sci 164:1111–1117

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tokunaga T, Miyahara K, Tabata K, Esaka M (2005) Generation, and properties of ascorbic acid-overproducing transgenic tobacco cells expressing sense RNA for L-galactono-1,4-lactone dehydrogenase. Planta 220:854–863

    Article  CAS  PubMed  Google Scholar 

  • Valpuesta V, Botella MA (2004) Biosynthesis of L-ascorbic acid in plants: new pathways for an old antioxidant. Trends Pant Sci 9:573–577

    Article  CAS  Google Scholar 

  • Vamos-Vigyazo L (1981) Polyphenol oxidase and peroxidase in fruits and vegetables. Crit Rev Food Sci Nutr 15:49–127

    Article  CAS  PubMed  Google Scholar 

  • von Heije G (1986) Mitochondrial targeting sequences may form amphiphilic helices. EMBO J 5:1335–1342

    Google Scholar 

  • Walker JRL (1995) Enzymatic browning in fruits: its biochemistry and control. In: Lee CY, Whitaker JR (eds) Enzymatic browning and its prevention. ASC symposium series 600, Washington, DC, pp 8–22

  • Wang J, Yu Y, Zhang Z, Quan R, Zhang H, Ma L, Deng XW, Huang R (2013) Arabidopsis CSN5B interacts with VTC1 and modulates ascorbic acid synthesis. Plant Cell 25:625–636

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369

    Article  CAS  PubMed  Google Scholar 

  • Wolucka BA, Persiau G, Van Doorsselaere J, Davey MW, Demol H, Vandekerckove J, Van Montagu M, Zabeau M, Boerjan W (2001) 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 98:14843–14848

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xu Y, Zhu X, Chen Y, Gong Y, Liu L (2013) Expression profiling of genes involved in ascorbate biosynthesis recycling during fleshy root development in radish. Plant Physiol Biochem 70:269–277

    Article  CAS  PubMed  Google Scholar 

  • Yu L, Jiang J, Zhang C, Jiang L, Ye N, Nu Y, Yang G, Liu E, Peng C, He Z, Peng X (2010) Glyoxylate rather than ascorbate is an efficient precursor of oxalate biosynthesis in rice. J Exp Bot 61:1625–1634

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang L, Wang Z, Xia Y, Kai G, Chen W, Tang K (2007) Metabolic engineering of plant L-ascorbic acid biosynthesis: recent trends and application. Crit Rev Biotechnol 27:173–182

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–166

    Google Scholar 

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Acknowledgments

We are indebted to Donato Giannino for providing the derivative binary vector pVDH282 and for the useful suggestions about transformation protocol of L. sativa.

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Authors and Affiliations

  1. Department of Agriculture, Food and Environment, University of Pisa, Via del Borghetto 80, 56124, Pisa, Italy

    Marco Landi, Marco Fambrini, Mariangela Salvini, Lucia Guidi & Claudio Pugliesi

  2. Interdepartmental Research Center “Nutraceuticals and Food for Health”, University of Pisa, Via del Borghetto 80, 56124, Pisa, Italy

    Lucia Guidi

  3. Institute of Life Sciences, Scuola Superiore Sant’Anna, Piazza Martiri della Libertà 33, 56127, Pisa, Italy

    Alice Basile

  4. Scuola Normale Superiore, Piazza dei Cavalieri 7, 56126, Pisa, Italy

    Mariangela Salvini

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  1. Marco Landi
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Correspondence to Claudio Pugliesi.

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Landi, M., Fambrini, M., Basile, A. et al. 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 Tiss Organ Cult 123, 109–120 (2015). https://doi.org/10.1007/s11240-015-0819-y

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