Regulation of fruit ascorbic acid concentrations during ripening in high and low vitamin C tomato cultivars

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Mellidou, Ifigeneia ^a   Keulemans, Johan ^a   Kanellis, Angelos K ^b   Davey, Mark W ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

Author keywords

Ascorbate biosynthesis; Ascorbate recycling; Ascorbate turnover; Candidate gene; GDP L galactose phosphorylase; Gene expression; Monodehydroascorbate reductase

Indexed keywords

LYCOPERSICON ESCULENTUM;

ASCORBIC ACID; GLUTATHIONE;

ARTICLE; BIOSYNTHESIS; CHEMISTRY; CLASSIFICATION; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; TOMATO;

ASCORBIC ACID; BIOSYNTHETIC PATHWAYS; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GLUTATHIONE; LYCOPERSICON ESCULENTUM;

MLCS; MLOWN;

EID: 84872596233     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-239     Document Type: Article

References (52)

1. Davey MW, Van Montagu M, Inze D, Sanmartin M, Kanellis A, Smirnoff N, Benzie IJJ, Strain JJ, Favell D, Fletcher J. Plant L-ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. J Sci Food Agric 2000, 80:825-860.
2. Smirnoff N, Conklin PL, Loewus FA. Biosynthesis of ascorbic acid in plants: A renaissance. Annual Rev Plant Physiol Plant Mol Biol 2001, 52:437-467.
3. Franck C, Baetens M, Lammertyn J, Verboven P. Davey MW. Nicolai BM: Ascorbic acid concentration in cv. conference pears during fruit development and postharvest storage. J Agric Food Chem 2003, 51:4757-4763.
4. Davey MW, Auwerkerken A, Keulemans J. Relationship of apple vitamin C and antioxidant contents to harvest date and postharvest pathogen infection. J Sci Food Agric 2007, 87:802-813.
5. Bulley S, Wright M, Rommens C, Yan H, Rassam M, Lin-Wang K, Andre C, Brewster D, Karunairetnam S, Allan AC, et al. Enhancing ascorbate in fruits and tubers through over-expression of the l-galactose pathway gene GDP-l-galactose phosphorylase. Plant Biotech J 2012, 10:390-397.
6. Diplock AT, Charleux JL, Crozier-Willi G, Kok FJ, Rice-Evans C, Roberfroid M, Stahl W, Vina-Ribes J. Functional food science and defence against reactive oxidative species. Br J Nutr 1998, 80:77-112.
7. Wheeler GLJM, Smirnoff N. The biosynthetic pathway of vitamin C in higher plants. Nature 1998, 393:365-369. 10.1038/30728, 9620799.
8. Conklin PL, Gatzek S, Wheeler GL, Dowdle J, Raymond MJ, Rolinski S, Isupov M, Littlechild JA, Smirnoff N. Arabidopsis thaliana VTC4 encodes L-galactose-1-P phosphatase, a plant ascorbic acid biosynthetic enzyme. J Biol Chem 2006, 281:15662-15670. 10.1074/jbc.M601409200, 16595667.
9. Bulley SM, Rassam M, Hoser D, Otto W, Schuenemann N, Wright M, MacRae E, Gleave A, Laing W. 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 2009, 60:765-778. 10.1093/jxb/ern327, 2652059, 19129165.
10. Mellidou I, Chagné D, Laing W, Keulemans J, Davey MW. Allelic variation in paralogs of GDP-L-galactose phosphorylase is a major determinant of vitamin C concentrations in apple fruit. Plant Physiol 2012, 160:1613-1629. 10.1104/pp.112.203786, 3490610, 23001142.
11. Ioannidi E, Kalamaki MS, Engineer C, Pateraki I, Alexandrou D, Mellidou I, Giovannonni J, Kanellis AK. Expression profiling of ascorbic acid-related genes during tomato fruit development and ripening and in response to stress conditions. J Exp Bot 2009, 60:663-678. 10.1093/jxb/ern322, 2651456, 19129160.
12. Gilbert L, Alhagdow M, Nunes-Nesi A, Quemener B, Guillon F, Bouchet B, Faurobert M, Gouble B, Page D, Garcia V, et al. 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 2009, 60:499-508. 10.1111/j.1365-313X.2009.03972.x, 19619161.
13. Davey MW, Gilot C, Persiau G, Ostergaard J, Han Y, Bauw GC, Van Montagu MC. Ascorbate biosynthesis in Arabidopsis cell suspension culture. Plant Physiol 1999, 121:535-543. 10.1104/pp.121.2.535, 59416, 10517845.
14. Agius F, Gonzalez-Lamothe R, Caballero JL, Munoz-Blanco J, Botella MA, Valpuesta V. Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase. Nat Biotechnol 2003, 21:177-181. 10.1038/nbt777, 12524550.
15. Wolucka BA, Van Montagu M. 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 2003, 278:47483-47490. 10.1074/jbc.M309135200, 12954627.
16. Lorence A, Chevone BI, Mendes P, Nessler CL. Myo-inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiol 2004, 134:1200-1205. 10.1104/pp.103.033936, 389944, 14976233.
17. Cruz-Rus E, Amaya I, Sanchez-Sevilla JF, Botella MA, Valpuesta V. Regulation of L-ascorbic acid content in strawberry fruits. J Exp Bot 2011, 62:4191-4201. 10.1093/jxb/err122, 3153677, 21561953.
18. Badejo AA, Wada K, Gao Y, Maruta T, Sawa Y, Shigeoka S, Ishikawa T. 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 2011, 63:229-239. 3245467, 21984649.
19. Foyer CH, Noctor G. Ascorbate and Glutathione: The Heart of the Redox Hub. Plant Physiol 2011, 155:2-18. 10.1104/pp.110.167569, 3075780, 21205630.
20. Chen ZYT, Ling J, Chang SC, Gallie DR. Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci U S A 2003, 100:3525-3530. 10.1073/pnas.0635176100, 152326, 12624189.
21. Eltayeb AEKN, Badawi GH, Kaminaka H, Sanekata T, Shibahara T, Inanaga S, Tanaka K. Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta 2007, 225:1255-1264. 10.1007/s00425-006-0417-7, 17043889.
22. Stevens R, Buret M, Duffe P, Garchery C, Baldet P, Rothan C, Causse M. Candidate genes and quantitative trait loci affecting fruit ascorbic acid content in three tomato populations. Plant Physiol 2007, 143:1943-1953. 10.1104/pp.106.091413, 1851805, 17277090.
23. Stevens R, Page D, Gouble B, Garchery C, Zamir D, Causse M. Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant Cell Environ 2008, 31:1086-1096. 10.1111/j.1365-3040.2008.01824.x, 18433441.
24. Haroldsen VM, Chi-Ham CL, Kulkarni S, Lorence A, Bennett AB. Constitutively expressed DHAR and MDHAR influence fruit, but not foliar ascorbate levels in tomato. Plant Physiol Biochem 2011, 49:1244-1249. 10.1016/j.plaphy.2011.08.003, 3310224, 21875809.
25. Mellidou I, Siomos A, Gerasopoulos D. Fruit composition and metabolism of 'Santorini', 'Chiou', 'Limnou' and 'Ailsa Craig' tomatoes 2005, Greece: Santorini, 2nd International Conference on Cherry Tomato 9-11 June 2005 2005.
26. Massot C, Stevens R, Genard M, Longuenesse J-J, Gautier H. Light affects ascorbate content and ascorbate-related gene expression in tomato leaves more than in fruits. Planta 2011, 235:153-163.
27. Hancock RD, Walker PG, Pont SDA, Marquis N, Vivera S, Gordon SL, Brennan RM, Viola R. L-Ascorbic acid accumulation in fruit of Ribes nigrum occurs by in situ biosynthesis via the L-galactose pathway. Funct Plant Biol 2007, 34:1080-1091.
28. Davey MW, Franck C, Keulemans J. Distribution, developmental and stress responses of antioxidant metabolism in Malus. Plant Cell Environ 2004, 27:1309-1320.
29. Pallanca J, Smirnoff N. The control of ascorbic acid synthesis and turnover in pea seedlings. J Exp Bot 2000, 51:669-674. 10.1093/jexbot/51.345.669, 10938858.
30. Bustin SA. Why the need for qPCR publication guidelines?-The case for MIQE. Methods 2009, 50:217-226.
31. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3:H0034.
32. Dumas Y, Dadomo M, Di Lucca G, Grolier P. Effects of environmental factors and agricultural techniques on antioxidant content of tomatoes. J Sci Food Agric 2003, 83:369-382.
33. Jimenez A, Creissen G, Kular B, Firmin J, Robinson S, Verhoeyen M, Mullineaux P. Changes in oxidative processes and components of the antioxidant system during tomato fruit ripening. Planta 2002, 214:751-758. 10.1007/s004250100667, 11882944.
34. Gautier H, Massot C, Stevens R, Serino S, Genard M. Regulation of tomato fruit ascorbate content is more highly dependent on fruit irradiance than leaf irradiance. Ann Bot 2009, 103:495-504. 2707328, 19033285.
35. Alhagdow M, Mounet F, Gilbert L, Nunes-Nesi A, Garcia V, Just D, Petit J, Beauvoit B, Fernie AR, Rothan C, et al. Silencing of the mitochondrial ascorbate synthesizing enzyme L-galactono-1,4-lactone dehydrogenase affects plant and fruit development in tomato. Plant Physiol 2007, 145:1408-1422. 10.1104/pp.107.106500, 2151702, 17921340.
36. Horemans N, Szarka A, De Bock M, Raeymaekers T, Potters G, Levine M, Banhegyi G, Guisez Y. Dehydroascorbate and glucose are taken up into Arabidopsis thaliana cell cultures by two distinct mechanisms. FEBS Lett 2008, 582:2714-2718. 10.1016/j.febslet.2008.07.001, 2751764, 18619442.
37. Horemans N, Asard H, Caubergs RJ. The ascorbate carrier of higher plant plasma membranes preferentially translocates the fully oxidized (dehydroascorbate) molecule. Plant Physiol 1997, 114(4):1247-1253. 158417, 12223769.
38. Hancock RD, McRae D, Haupt S, Viola R. Synthesis of L-ascorbic acid in the phloem. BMC Plant Biol 2003, 3:7. 10.1186/1471-2229-3-7, 317296, 14633288.
39. Razavi F, Keulemans J, Davey MW. A study of the L-ascorbate biosynthetic capacity of apple fruit. Commun Agric Appl Biol Sci 2005, 70:213-216.
40. Li M-J, Ma F-W, Zhang M, Pu F. Distribution and metabolism of ascorbic acid in apple fruits (Malus domestica Borkh cv. Gala). Plant Sci 2008, 174:606-612.
41. Mieda T, Yabuta Y, Rapolu M, Motoki T, Takeda T, Yoshimura K, Ishikawa T, Shigeoka S. Feedback inhibition of spinach L-galactose dehydrogenase by L-ascorbate. Plant Cell Physiol 2004, 45:1271-1279. 10.1093/pcp/pch152, 15509850.
42. Arrigoni O, Calabrese G, DeGara L, Bitonti MB, Liso R. Correlation between changes in cell ascorbate and growth of Lupinus albus seedlings. J Plant Physiol 1997, 150:302-308.
43. Linster CL, Clarke SG. L-Ascorbate biosynthesis in higher plants: the role of VTC2. Trends Plant Sci 2008, 13:567-573. 10.1016/j.tplants.2008.08.005, 2583178, 18824398.
44. Davey MW, Dekempeneer E, Keulemans J. Rocket-powered high-performance liquid chromatographic analysis of plant ascorbate and glutathione. Anal Biochem 2003, 316:74-81. 10.1016/S0003-2697(03)00047-2, 12694729.
45. Bradford MM. Rapid and sensitive method for quantification of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.
46. Nakano Y, Asada K. Purification of ascorbate peroxidase in spinach-chloroplasts - its inactivation in ascornate-depleted medium and reactivation by monodehydroascorbate radical. Plant Cell Physiol 1987, 28:131-140.
47. Arrigoni O, Dipierro S, Borraccino G. Ascorbate free-radical reductase, a key enzyme of the ascorbic-acid system. FEBS Lett 1981, 125:242-244.
48. Edwards EA, Rawsthorne S, Mullineaux PM. Subcellular-istribution of multiple forms of glutathione-reductase in leaves of pea (Pisum sativum L.). Planta 1990, 180:278-284.
49. Chance B, Maehly AC. Assay of catalase and peroxidase. Methods Enzymol 1955, 2:764-775.
50. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A. Geneious v5.4 2011 Available from http://www.geneious.com/.
51. Gasic K, Hernandez A, Korban SS. RNA extraction from different apple tissues rich in polyphenols and polysaccharides for cDNA library construction. Plant Mol Biol Rep 2004, 22:437-438.
52. Pfaffl MW. The ongoing evolution of qPCR. Methods 2010, 50:215-216. 10.1016/j.ymeth.2010.02.005, 20215019.