Increased antioxidant capacity in tomato by ectopic expression of the strawberry D-galacturonate reductase gene

Biotechnology Journal

Volumn 10, Issue 3, 2015, Pages 490-500

  Amaya, Iraida ^a   Osorio, Sonia ^b,c   Martinez Ferri, Elsa ^a   Lima Silva, Viviana ^c   Doblas, Veronica G ^c   Fernández Muñoz, Rafael ^c   Fernie, Alisdair R ^b   Botella, Miguel A ^c   Valpuesta, Victoriano ^c  

^a IFAPA CENTRO EL TORUÑO   (Spain)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c INSTITUTO DE HORTOFRUTICULTURA SUBTROPICAL Y MEDITERRÁNEA LA MAYORA   (Spain)

Author keywords

Antioxidants; Ascorbic acid; Galacturonate reductase; Redox; Solanum lycopersicum

Indexed keywords

AGENTS; AMINO ACIDS; ANTIOXIDANTS; ASCORBIC ACID; BIOCHEMISTRY; BIOSYNTHESIS; C (PROGRAMMING LANGUAGE); GENE EXPRESSION; GENES; GENETIC ENGINEERING; METABOLISM; METABOLITES; MOBILE SECURITY; ORGANIC ACIDS; PLANTS (BOTANY); QUENCHING;

ANTIOXIDANT CAPACITY; D GALACTURONIC ACIDS; GALACTURONATE REDUCTASE; METABOLOMIC ANALYSIS; NON-PHOTOCHEMICAL FLUORESCENCE QUENCHING; REDOX; SOLANUM LYCOPERSICUM; TOTAL ANTIOXIDANT CAPACITY;

FRUITS;

ASCORBIC ACID; ASPARAGINE; CHLOROGENIC ACID; CHLOROPHYLL; CITRIC ACID; DEXTRO GALACTURONATE REDUCTASE; FRUCTOSE; GALACTAN; GALACTINOL; GLUCOSE; GLUTAMIC ACID; OXIDOREDUCTASE; SUCROSE; UNCLASSIFIED DRUG; ALCOHOL DEHYDROGENASE; ANTIOXIDANT; D-GALACTURONATE REDUCTASE;

ANTIOXIDANT ACTIVITY; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; FLUORESCENCE; FRUIT; GENE EXPRESSION; NONPHOTOCHEMICAL QUENCHING; PLANT LEAF; PRIORITY JOURNAL; PROMOTER REGION; STRAWBERRY; TOMATO; TRANSGENIC CROP; ECTOPIC EXPRESSION; ENZYMOLOGY; FRAGARIA; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; METABOLOMICS; PLANT GENE; PROCEDURES; TRANSGENIC PLANT;

FRAGARIA X ANANASSA; LYCOPERSICON ESCULENTUM;

ANTIOXIDANTS; ASCORBIC ACID; ECTOPIC GENE EXPRESSION; FRAGARIA; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HUMANS; LYCOPERSICON ESCULENTUM; METABOLOMICS; NAD (+) AND NADP (+) DEPENDENT ALCOHOL OXIDOREDUCTASES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC;

EID: 84924431611     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201400279     Document Type: Article

References (64)

1. Nishikimi, M., Fukuyama, R., Minoshima, S., Shimizu, N., Yagi, K., Cloning and chromosomal mapping of the human nonfunctional gene for L-gulono-gamma-lactone oxidase, the enzyme for L-ascorbic acid biosynthesis missing in man. J. Biol. Chem. 1994, 269, 13685-13688.
2. Li, Y., Schellhorn, H. E., New developments and novel therapeutic perspectives for vitamin C. J. Nutr. 2007, 137, 2171-2184.
3. Valpuesta, V., Botella, M. A., Biosynthesis of L-ascorbic acid in plants: New pathways for an old antioxidant. Trends Plant Sci. 2004, 9, 573-577.
4. Foyer, C. H., Noctor, G., Ascorbate and glutathione: The heart of the redox hub. Plant Physiol. 2011, 155, 2-18.
5. Cruz-Rus, E., Amaya, I., Valpuesta, V., The challenge of increasing vitamin C content in plant foods. Biotechnol. J. 2012, 7, 1110-1121.
6. Foyer, C. H., Shigeoka, S., Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol. 2011, 155, 93-100.
7. Smirnoff, N., Ascorbic acid: Metabolism and functions of a multi-facetted molecule. Curr. Opin. Plant Biol. 2000, 3, 229-235.
8. Tabata, K., Ôba, K., Suzuki, K., Esaka, M., Generation and properties of ascorbic acid-deficient transgenic tobacco cells expressing antisense RNA for L-galactono-1, 4-lactone dehydrogenase. Plant J. 2001, 27, 139-148.
9. Borraccino, G., Mastropasqua, L., De Leonardis, S., Dipierro, S., The role of the ascorbic acid system in delaying the senescence of oat (Avena sativa L.) leaf segments. J. Plant Physiol. 1994, 144, 161-166.
10. Barth, C., Moeder, W., Klessig, D. F., Conklin, P. L., The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-1. Plant Physiol. 2004, 134, 1784-1792.
11. Pavet, V., Olmos, E., Kiddle, G., Mowla, S. et al., Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis. Plant Physiol. 2005, 139, 1291-1303.
12. Pastori, G. M., Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 2003, 15, 939-951.
13. Franck, C., Baetens, M., Lammertyn, J., Verboven, P. et al., Ascorbic acid concentration in Cv. conference pears during fruit development and postharvest storage. J. Agric. Food Chem. 2003, 51, 4757-4763.
14. Davey, M. W., 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.
15. Bulley, S., Wright, M., Rommens, C., Yan, H. et al., Enhancing ascorbate in fruits and tubers through over-expression of the L-galactose pathway gene GDP-l-galactose phosphorylase. Plant Biotechnol. J. 2012, 10, 390-397.
16. Fitzpatrick, T. B., Basset, G. J. C., Borel, P., Carrari, F. et al., Vitamin deficiencies in humans: Can plant science help? Plant Cell 2012, 24, 395-414.
17. Ishikawa, T., Dowdle, J., Smirnoff, N., Progress in manipulating ascorbic acid biosynthesis and accumulation in plants. Physiol Plant. 2006, 126, 343-355.
18. Wheeler, G. L., Jones, M. A., Smirnoff, N., The biosynthetic pathway of vitamin C in higher plants. Nature 1998, 393, 365-369.
19. Wolucka, B. A., 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.
20. Agius, F., González-Lamothe, R., Caballero, J. L., Muñoz-Blanco, J. et al., Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase. Nat. Biotechnol. 2003, 21, 177-181.
21. Zhang, C., Liu, J., Zhang, Y., Cai, X. et al., Overexpression of SlGMEs leads to ascorbate accumulation with enhanced oxidative stress, cold, and salt tolerance in tomato. Plant Cell Rep. 2011, 30, 389-398.
22. Carrari, F., Baxter, C., Usadel, B., Urbanczyk-Wochniak, E. et al., 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 Physiol. 2006, 142, 1380-1396.
23. Cruz-Rus, E., Amaya, I., Sánchez-Sevilla, J. F., Botella, M. A., Valpuesta, V., Regulation of L-ascorbic acid content in strawberry fruits. J. Exp. Bot. 2011, 62, 4191-4201.
24. Hemavathi, A., Upadhyaya, C. P., Akula, N., Young, K. E. et al., Enhanced ascorbic acid accumulation in transgenic potato confers tolerance to various abiotic stresses. Biotechnol. Lett. 2010, 32, 321-330.
25. Ioannidi, E., Kalamaki, M. S., Engineer, C., Pateraki, I. et al., 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.
26. Badejo, A., Wada, K., Gao, Y., Maruta, T. et al., 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. 2012, 63, 229-239.
27. Gonzalez-Bosch, C., Brummell, D. A., Bennett, A. B., Differential expression of two endo-1, 4-[beta]-glucanase genes in pericarp and locules of wild-type and mutant tomato fruit. Plant Physiol. 1996, 111, 1313-1319.
28. Van Engelen, F.A., Molthoff, J.W., Conner, A.J., Nap, J.P. et al., pBINPLUS: An improved plant transformation vector based on pBIN19. Transgenic Res. 1995, 4, 288-290.
29. Nicholass, F. J., Smith, C. J., Schuch, W., Bird, C. R., Grierson, D., High levels of ripening-specific reporter gene expression directed by tomato fruit polygalacturonase gene-flanking regions. Plant Mol. Biol. 1995, 28, 423-435.
30. Ditta, G., Stanfield, S., Corbin, D., Helinski, D. R., Broad host range DNA cloning system for gram-negative bacteria: Construction of a gene bank of Rhizobium meliloti. Proc. Natl. Acad. Sci. USA 1980, 77, 7347-7351.
31. Ellul, P., Garcia-Sogo, B., Pineda, B., Rios, G. et al., The ploidy level of transgenic plants in Agrobacterium-mediated transformation of tomato cotyledons (Lycopersicon esculentum L. Mill.) is genotype and procedure dependent. Theor. Appl. Genet. 2003, 106, 231-238.
32. Doyle, J. J., Doyle, J. L., Isolation of plant DNA from fresh tissue. Focus 1990, 12, 13-15.
33. Lima-Silva, V., Rosado, A., Amorin-Silva, V., Muñoz-Mérida, A. et al., Genetic and genome-wide transcriptomic analyses identify co-regulation of oxidative response and hormone transcript abundance with vitamin c content in tomato fruit. BMC Genomics 2012, 13, 187.
34. Davey, M. W., Dekempeneer, E., Keulemans, J., Rocket-powered high-performance liquid chromatographic analysis of plant ascorbate and glutathione. Anal. Biochem. 2003, 316, 74-81.
35. Pellegrini, N., Re, R., Yang, M., Rice-Evans, C., Screening of dietary carotenoids and carotenoid-rich fruit extracts for antioxidant activities applying 2, 2'-azinobis(3-ethylenebenzothiazoline-6-sulfonic acid radical cation decolorization assay. Methods Enzymol. 1999, 299, 379-389.
36. Re, R., Pellegrini, N., Proteggente, A., Pannala, A. et al., Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 1999, 26, 1231-1237.
37. Osorio, S., Do, P. T., Fernie, A. R., Profiling primary metabolites of tomato fruit with gas chromatography/mass spectrometry. Methods Mol. Biol. 2012, 860, 101-109.
38. Luedemann, A., Strassburg, K., Erban, A., Kopka, J., TagFinder for the quantitative analysis of gas chromatography-mass spectrometry (GC-MS)-based metabolite profiling experiments. Bioinformatics 2008, 24, 732-737.
39. Schreiber, U., Bilger, W., Neubauer, C., Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. in: Schulze, E. D., Caldwell, M. M. (Eds.), Ecophysiology of Photosynthesis, Springer, Berlin 1994, pp. 49-70.
40. Klughammer, C., Schreiber, U., Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. PAM Appl. Notes 2008, 1, 27-35.
41. Kramer, D. M., Johnson, G., Kiirats, O., Edwards, G. E., New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth. Res. 2004, 79, 209-218.
42. Klee, H. J., Giovannoni, J. J., Genetics and control of tomato fruit ripening and quality attributes. Annu. Rev. Genet. 2011, 45, 41-59.
43. Foyer, C. H., Noctor, G., Redox regulation in photosynthetic organisms: Signaling, acclimation, and practical implications. Antioxid. Redox Signal. 2009, 11, 861-905.
44. Sweetlove, L. J., Beard, K. F. M., Nunes-Nesi, A., Fernie, A. R., Ratcliffe, R. G., Not just a circle: Flux modes in the plant TCA cycle. Trends Plant Sci. 2010, 15, 462-470.
45. Maxwell, K., Johnson, G. N., Chlorophyll fluorescence - a practical guide. J. Exp. Bot. 2000, 51, 659-668.
46. Mellidou, I., Keulemans, J., Kanellis, A. K., Davey, M. W., Regulation of fruit ascorbic acid concentrations during ripening in high and low vitamin C tomato cultivars. BMC Plant Biol. 2012, 12, 239.
47. Alhagdow, M., Mounet, F., Gilbert, L., Nunes-Nesi, A. 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.
48. Liu, W., An, H.-M., Yang, M., Overexpression of Rosa roxburghii l-galactono-1, 4-lactone dehydrogenase in tobacco plant enhances ascorbate accumulation and abiotic stress tolerance. Acta Physiol. Plant. 2013, 35, 1617-1624.
49. Tokunaga, T., Miyahara, K., Tabata, K., Esaka, M., Generation and properties of ascorbic acid-overproducing transgenic tobacco cells expressing sense RNA for l-galactono-1, 4-lactone dehydrogenase. Planta 2004, 220, 854-863.
50. Schauer, N., Zamir, D., Fernie, A. R., Metabolic profiling of leaves and fruit of wild species tomato: A survey of the Solanum lycopersicum complex. J. Exp. Bot. 2005, 56, 297-307.
51. Araujo, W. L., Tohge, T., Osorio, S., Lohse, M. et al., Antisense inhibition of the 2-oxoglutarate dehydrogenase complex in tomato demonstrates its importance for plant respiration and during leaf senescence and fruit maturation. Plant Cell 2012, 24, 2328-2351.
52. Sienkiewicz-Porzucek, A., Sulpice, R., Osorio, S., Krahnert, I. et al., Mild reductions in mitochondrial NAD-dependent isocitrate dehydrogenase activity result in altered nitrate assimilation and pigmentation but do not impact growth. Mol. Plant 2010, 3, 156-173.
53. Centeno, D. C., Osorio, S., Nunes-Nesi, A., Bertolo, A. L. F. et al., Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening. Plant Cell 2011, 23, 162-184.
54. Garchery, C., Gest, N., Do, P. T., Alhagdow, M. et al., A diminution in ascorbate oxidase activity affects carbon allocation and improves yield in tomato under water deficit. Plant Cell Environ. 2013, 36, 159-175.
55. Downie, B., Expression of a GALACTINOL SYNTHASE gene in tomato seeds is up-regulated before maturation desiccation and again after imbibition whenever radicle protrusion is prevented. Plant Physiol. 2003, 131, 1347-1359.
56. Karner, U., myo-Inositol and sucrose concentrations affect the accumulation of raffinose family oligosaccharides in seeds. J. Exp. Bot. 2004, 55, 1981-1987.
57. Nishizawa, A., Yabuta, Y., Shigeoka, S., Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 2008, 147, 1251-1263.
58. Niggeweg, R., Michael, A. J., Martin, C., Engineering plants with increased levels of the antioxidant chlorogenic acid. Nat. Biotechnol. 2004, 22, 746-754.
59. Luo, J., Butelli, E., Hill, L., Parr, A. et al., AtMYB12 regulates caffeoyl quinic acid and flavonol synthesis in tomato: Expression in fruit results in very high levels of both types of polyphenol. Plant J. 2008, 56, 316-326.
60. Winkel-Shirley, B., Biosynthesis of flavonoids and effects of stress. Curr. Opin. Plant Biol. 2002, 5, 218-223.
61. Kratzer, R., Wilson, D. K., Nidetzky, B., Catalytic mechanism and substrate selectivity of aldo-keto reductases: Insights from structure-function studies of Candida tenuis xylose reductase. IUBMB Life 2006, 58, 499-507.
62. Kasajima, I., Takahara, K., Kawai-Yamada, M., Uchimiya, H., Estimation of the relative sizes of rate constants for chlorophyll de-excitation processes through comparison of inverse fluorescence intensities. Plant Cell Physiol. 2009, 50, 1600-1616.
63. Dall'Osto, L., A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. Plant Cell 2005, 17, 1217-1232.
64. Nunes-Nesi, A., Araujo, W. L., Fernie, A. R., Targeting mitochondrial metabolism and machinery as a means to enhance photosynthesis. Plant Physiol. 2011, 155, 101-107.