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

Journal of Experimental Botany

Volumn 63, Issue 1, 2012, Pages 229-239

  Badejo, Adebanjo Ayobamidele ^a,c   Wada, Keiko ^a   Gao, Yongshun ^a   Maruta, Takanori ^a   Sawa, Yoshihiro ^a   Shigeoka, Shigeru ^b   Ishikawa, Takahiro ^a  

^a SHIMANE UNIVERSITY   (Japan)

^b KINKI UNIVERSITY   (Japan)

^c FEDERAL UNIVERSITY OF TECHNOLOGY   (Nigeria)

Author keywords

Ascorbate biosynthesis; D galacturonate pathway; D mannose L galactose pathway; tomato fruits; translocation

Indexed keywords

ASCORBIC ACID; GALACTOSE; GALACTURONIC ACID; HEXURONIC ACID; MANNOSE; PRIMER DNA;

ARTICLE; AUTORADIOGRAPHY; DRUG EFFECT; ELECTRON TRANSPORT; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NUCLEOTIDE SEQUENCE; PHOTOSYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; TOMATO; TRANSPORT AT THE CELLULAR LEVEL;

ASCORBIC ACID; AUTORADIOGRAPHY; BASE SEQUENCE; BIOLOGICAL TRANSPORT; DNA PRIMERS; ELECTRON TRANSPORT; GALACTOSE; HEXURONIC ACIDS; LYCOPERSICON ESCULENTUM; MANNOSE; PHOTOSYNTHESIS; REAL-TIME POLYMERASE CHAIN REACTION;

LYCOPERSICON ESCULENTUM;

EID: 84555206990     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err275     Document Type: Article

References (47)

1. Agius F, Gonzalez-Lamonthe R, Caballero JL, Munoz-Blanco J, Botella MA, Valpuesta V. 2003. Engineering increased vitamin C levels in plants by over-expression of a D-galacturonic acid reductase. Nature Biotechnology 21, 177-181.
2. Aoki K, Yano K, Suzuki A, et al. 2010. Large-scale analysis of full-length cDNAs from the tomato (Solanum lycopersicum) cultivar Micro-Tom, a reference system for the Solanaceae genomics. BMC Genomics 11, 210.
3. Badejo AA, Fujikawa Y, Esaka M. 2009. Gene expression of ascorbic acid biosynthesis related enzymes of the Smirnoff-Wheeler pathway in acerola (Malpighia glabra). Journal of Plant Physiology 166, 652-660.
4. Barth C, Moeder W, Klessig DF, Conklin PL. 2004. The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin C-1. Plant Physiology 134, 1784-1792.
5. Bulley SM, Rassam M, Hoser D, Otto W, Schunemann N, Wright M, MacRae E, Gleave A, Laing W. 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. Journal of Experimental Botany 60, 765-778.
6. Carrari F, Baxter C, Usadel B, et al. 2006. Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiology 142, 1380-1396.
7. Chinoy NJ. 1969. On the specificity of the alcoholic, acidic silver nitrate reagent for the histochemical localization of ascorbic acid. Histochemie 20, 105-107.
8. Conklin PL, Norris SR, Wheeler GL, Williams EH, Smirnoff N, Last RL. 1999. Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) biosynthesis. Proceedings of the National Academy of Sciences, USA 96, 4198-4203.
9. 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. Journal of Plant Physiology 167, 739-748.
10. Davies JN, Hobson GE. 1981. The constituents of tomato fruit-the influence of environment, nutrition, and genotype. Critical Reviews in Food Science and Nutrition 15, 205-280.
11. Davey MD, Van Montagu M, Inze D, Sanmartin M, Kanellis AK, Smirnoff N, Benzie IJJ, Strain JJ, Favel D, Fletcher J. 2000. Plant L-ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. Journal of the Science of Food and Agriculture 80, 825-860.
12. Debolt S, Melino V, Ford CM. 2007. Ascorbate as a biosynthetic precursor in plants. Annals of Botany 99, 3-8.
13. Di Matteo A, Sacco A, Anacleria M, Pezzotti M, Delledonne M, Ferrarini A, Frusciante L, Barone A. 2010. The ascorbic acid content of tomato fruits is associated with the expression of genes involved in pectin degradation. BMC Plant Biology 10, 163.
14. 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. The Plant Journal 52, 673-689.
15. Dumville JC, Fry SC. 2003. Solubilisation of tomato fruit pectins by ascorbate: a possible non-enzymic mechanism of fruit softening. Planta 217, 951-961.
16. Foyer CH, Shigeoka S. 2011. Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiology 155, 93-100.
17. Franceschi VR, Tarlyn NM. 2002. l-Ascorbic acid is accumulated in source leaf phloem and transported to sink tissues in plants. Plant Physiology 130, 649-656.
18. Gautier H, Massot C, Stevens R, Serino S, Genard M. 2009. Regulation of tomato fruit ascorbate content is more highly dependent on fruit irradiance than leaf irradiance. Annals of Botany 103, 495-504.
19. Hanson J, Smeekens S. 2009. Sugar perception and signaling-an update. Current Opinion in Plant Biology 12, 562-567.
20. Hayashi H, Chino M. 1990. Chemical composition of phloem sap from the uppermost internode of the rice plant. Plant and Cell Physiology 31, 247-251.
21. 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. Physiologia Plantarum 136, 139-149.
22. 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. Journal of Experimental Botany 60, 663-678.
23. Ishikawa T, Dowdle J, Smirnoff N. 2006a. Progress in manipulating ascorbic acid biosynthesis and accumulation in plants. Physiologia Plantarum 126, 343-355.
24. Ishikawa T, Masumoto I, Iwasa N, Nishikawa H, Sawa Y, Shibata H, Nakamura A, Yabuta Y, Shigeoka S. 2006b. Functional characterization of D-galacturonic acid reductase, a key enzyme of the ascorbate biosynthesis pathway. from Euglena gracilis. Bioscience, Biotechnology, and Biochemistry 70, 2720-2726.
25. Ishikawa T, Nishikawa H, Gao Y, Sawa Y, Shibata H, Yabuta Y, Maruta T, Shigeoka S. 2008. The pathway via D-galacturonate/L-galactonate is significant for ascorbate biosynthesis in Euglena gracilis: identification and functional characterization of aldonolactonase. Journal of Biological Chemistry 283, 31133-31141.
26. Ishikawa T, Shigeoka S. 2008. Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Bioscience, Biotechnology, and Biochemistry 72, 1143-5114.
27. Jimenez A, Creissen G, Kular B, Firmin J, Robinson S, Verhoeyen M, Mullineaux P. 2002. Changes in oxidative processes and components of the antioxidant system during tomato fruit ripening. Planta 214, 751-758.
28. Kampfenkel K, Van Montagu M, Inze D. 1995. Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Analytical Biochemistry 225, 165-167.
29. Kondo Y, Inai Y, Sato Y, Handa S, Kubo S, Shimokado K, Goto S, Nishikimi M, Maruyama N, Ishigami A. 2006. Senescence marker protein 30 functions as gluconolactonase in L-ascorbic acid biosynthesis, and its knockout mice are prone to scurvy. Proceedings of the National Academy of Sciences, USA 103, 5723-8572.
30. Linster CL, Clarke SG. 2008. l-Ascorbate biosynthesis in higher plants: the role of VTC2. Trends in Plant Science 13, 567-573.
31. Loewus FA, Kelly S. 1961a. Identity of l-ascorbic acid formed from d-glucose by the strawberry (Fragaria). Nature 191, 1059-1061.
32. Loewus FA, Kelly S. 1961b. The metabolism of D-galacturonic acid and its methyl ester in the detached ripening strawberry. Archives of Biochemistry and Biophysics 95, 483-493.
33. Lorence A, Chevone BI, Mendes P, Nessler C. 2004. myo-inositol oxygenase offers a possible entry point into plant AsA biosynthesis. Plant Physiology 134, 1200-1205.
34. Massot C, Genard M, Stevens R, Gautier H. 2010. Fluctuations in sugar content are not determinant in explaining variations in vitamin C in tomato fruit. Plant Physiology and Biochemistry 48, 751-757.
35. Mieda T, Yabuta Y, Rapolu M, Motoki T, Takeda T, Yoshimura K, Ishikawa T, Shigeoka S. 2004. Feedback inhibition of spinach L-galactose dehydrogenase by L-ascorbate. Plant and Cell Physiology 45, 1271-1279.
36. Melino VJ, Soole KL, Ford CM. 2009. Ascorbate metabolism and the developmental demand for tartaric and oxalic acids in ripening grape berries. BMC Plant Biology 9, 145.
37. Nishikawa F, Kato M, Hyodo H, Ikoma Y, Sugiura M, Yano M. 2005. Effect of sucrose on ascorbate level and expression of genes involved in the ascorbate biosynthesis and recycling pathway in harvested broccoli florets. Journal of Experimental Botany 56, 65-72.
38. Noctor G. 2006. Metabolic signaling in defence and stress: the central roles of soluble redox couples. Plant, Cell and Environment 29, 409-425.
39. Pfannschmidt T, Nilsson A, Allen JF. 1999. Photosynthetic control of chloroplast gene expression. Nature 397, 625-628.
40. Shinagawa E, Ano Y, Yakushi T, Adachi O, Matsushita K. 2009. Solubilization, purification, and properties of membrane-bound D-glucono-d-lactone hydrolase from. Gluconobacter oxydans. Bioscience, Biotechnology, and Biochemistry 73, 241-244.
41. Smirnoff N. 2000. Ascorbic acid: metabolism and functions of a multi-facetted molecule. Current Opinion in Plant Biology 3, 229-235.
42. Stevens R, Buret M, DufféP, Garchery C, Baldet P, Rothan C, Causse M. 2007. Candidate genes and quantitative trait loci affecting fruit ascorbic acid content in three tomato populations. Plant Physiology 143, 1943-1953.
43. Tedone L, Hancock RD, Alberino S, Haupt S, Viola R. 2004. Longdistance transport of L-ascorbic acid in potato. BMC Plant Biology 4, 16.
44. Wheeler GL, Jones MA, Smirnoff N. 1998. The biosynthetic pathway of vitamin C in higher plants. Nature 393, 365-369.
45. 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. Journal of Biological Chemistry 278, 47483-47490.
46. Yabuta Y, Mieda T, Rapolu M, Nakamura A, Motoki T, Maruta T, Yoshimura K, Ishikawa T, Shigeoka S. 2007. Light regulation of ascorbate biosynthesis is dependent on the photosynthetic electron transport chain but independent of sugars in Arabidopsis. Journal of Experimental Botany 58, 2661-2671.
47. Yabuta Y, Yoshimura K, Takeda T, Shigeoka S. 2000. Molecular characterization of tobacco mitochondrial L-galactono-gamma-lactone dehydrogenase and its expression in. Escherichia coli. Plant and Cell Physiology 41, 666-675.