Altered activity of the P2 isoform of plastidic glucose 6-phosphate dehydrogenase in tobacco (Nicotiana tabacum cv. Samsun) causes changes in carbohydrate metabolism and response to oxidative stress in leaves

Plant Journal

Volumn 38, Issue 1, 2004, Pages 49-59

  Debnam, Phillip M ^c   Fernie, Alisdair R ^b   Leisse, Andrea ^b   Golding, Alison ^c   Bowsher, Caroline G ^c   Grimshaw, Caroline ^c   Knight, Jacqueline S ^d   Emes, Michael J ^a  

^a UNIVERSITY OF GUELPH   (Canada)

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

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d Ag Research Wallaceville   (New Zealand)

Author keywords

Antioxidants; Carbohydrate; Chloroplasts; Glucose 6 phosphate dehydrogenase; Oxidative pentose phosphate pathway

Indexed keywords

ANTIOXIDANTS; CARBOHYDRATES; ENZYMES; METABOLISM; OXIDATION; STRESS ANALYSIS;

ISOFORMS; TRANSGENIC TOBACCO;

PLANTS (BOTANY);

COMPLEMENTARY DNA; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; ISOENZYME; PLANT DNA;

ARTICLE; CARBOHYDRATE METABOLISM; CHLOROPLAST; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHENOTYPE; PLANT LEAF; TOBACCO; TRANSGENIC PLANT;

BASE SEQUENCE; CARBOHYDRATE METABOLISM; CHLOROPLASTS; DNA, ANTISENSE; DNA, PLANT; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GLUCOSEPHOSPHATE DEHYDROGENASE; ISOENZYMES; OXIDATIVE STRESS; PHENOTYPE; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; TOBACCO;

BRASSICA OLERACEA VAR. BOTRYTIS; CAULIFLOWER MOSAIC VIRUS; EMBRYOPHYTA; EUKARYOTA; NICOTIANA; NICOTIANA TABACUM;

EID: 1842535076     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02017.x     Document Type: Article

References (44)

1. Apel, K. and Kloppstech, K. (1978) The plastid membrane of barley (Hordeum vulgare). Light-induced appearance of mRNA coding for apoprotein light harvesting chlorophyll a/b protein. Eur. J. Biochem. 85, 581-588.
2. Arakawa, N., Tsutsumi, K., Sauceda, N.G., Kurata, T. and Inagaki, C. (1981) A rapid and sensitive method for the determination of ascorbic acid using 4,7-diphenyl-1,10-phenanthroline. Agric. Biol. Chem. 45, 1289-1290.
3. Asada, K. (1984) Chloroplasts: formation of active oxygen and its scavenging. Meth. Enzymol. 105, 422-429.
4. Bevan, M. (1984) Binary Agrobacterium vectors for plant transformation. Nucl. Acids Res. 12, 8711-8721.
5. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein-dye binding. Anal. Biochem. 72, 248-254.
6. Brennan, T. and Anderson, L.E. (1980) Institution by catalase of dark-mediated glucose 6-phosphate dehydrogenase activation in pea chloroplasts. Plant Physiol. 66, 815-817.
7. Broadbent, P., Creissen, G.P., Kular, B., Wellburn, A.R. and Mullineaux, P.M. (1995) Oxidative stress responses in transgenic tobacco containing altered levels of glutathione reductase activity. Plant J. 8, 247-255.
8. 2 assimilation in oxygenic photosynthesis - the ferredoxin thioredoxin system - perspective on its discovery, present status, and future-development. Arch. Biochem. Biophys. 288, 1-9.
9. Creissen, G., Reynolds, H., Xue, Y. and Mullineaux, P. (1995) Simultaneous targeting of pea glutathione reductase and of a bacterial fusion protein to chloroplasts and mitochondria in transgenic tobacco. Plant J. 18, 167-175.
10. Creissen, G., Firmin, J., Fryer, M. et al. (1999) Elevated biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. Plant Cell, 11, 1277-1291.
11. Debnam, P.M. and Emes, M.J. (1999) Subcellular distribution of enzymes of the oxidative pentose phosphate pathway in root and leaf tissues. J. Exp. Bot. 50, 1653-1661.
12. Drincovich, M.F., Casati, P., Andreo, C.S., Donahue, R. and Edwards, G.E. (1998) UV-B induction of NADP-malic enzyme in etiolated and green maize seedlings. Plant Cell Environ. 21, 63-70.
13. Eicks, M., Maurino, V., Knappe, S., Flugge, U.I. and Fischer, K. (2002) The plastidic pentose phosphate translocator represents a link between the cytosolic and the plastidic pentose phosphate pathways in plants. Plant Physiol. 128, 512-522.
14. Fernie, A.R., Roessner, U., Trethewey, R.N. and Willmitzer, L. (2001) The contribution of plastidial phosphoglucomutase to the control of starch synthesis within the potato tuber. Planta, 213, 418-426.
15. Fischer, D.K. and Guiltinan, M.J. (1995) Rapid, efficient production of homozygous transgenic tobacco plants with Agrobacterium tumefaciens - a seed-to-seed protocol. Plant Mol. Biol. Rep. 13, 278-289.
16. Foyer, C.H. and Halliwell, B. (1976) The presence of glutathione and glutathione reductase in chloroplasts. A proposed role in ascorbic acid metabolism. Planta, 133, 21-25.
17. Fu, Y., Ballicora, M.A., Leykam, J.F. and Preiss, J. (1998) Mechanism of reductive activation of potato tuber ADP-glucose pyrophosphorylase. J. Biol. Chem. 273, 25045-25052.
18. Hendriks, J.H.M., Kolbe, A., Gibon, Y., Stitt, M. and Geigenberger, P. (2003) ADP-glucose pyrophosphorylase is activated by post-translational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol. 133, 1-12.
19. Hossain, M.A., Nakano, Y. and Asada, K. (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol. 25, 385-395.
20. Juhnke, H., Krems, B., Kotter, P. and Entian, K.D. (1996) Mutants that show increased sensibility to hydrogen peroxide reveal an important role for the pentose phosphate pathway in protection of yeast against oxidative stress. Mol. Gen. Genet. 252, 454-464.
21. Karpinski, S., Escobar, C., Karpinska, B., Creissen, G. and Mullineaux, P.M. (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell, 9, 627-640.
22. Karpinski, S., Reynolds, H., Karpinska, B., Wingsle, G., Creissen, G. and Mullineaux, P. (1999) Systemic signalling and acclimation in response to excess excitation energy. Science, 23, 654-657.
23. 2 content and antioxidants in maize (Zea mays) grown at sub-optimal temperatures. Plant Cell Environ. 22, 1071-1083.
24. Knight, J.S. and Emes, M.J. (1996) Isolation of a tobacco (Nicotiana tabacum) chloroplast glucose-6-phosphate dehydrogenase cDNA (Accession No. X99405). Plant Physiol. 112, 861.
25. Knight, J.S., Emes, M.J. and Debnam, P.M. (2001) Isolation and characterization of a full-length genomic clone encoding a plastidic glucose 6-phosphate dehydrogenase from Nicotiana tabacum. Planta, 212, 499-507.
26. Lahner, S.K., Kramer, V., Back, E., Privalle, L. and Rothstein, S. (1988) Molecular cloning of complementary DNA encoding maize nitrite reductase: molecular analysis and nitrate induction. Plant Physiol. 88, 741-774.
27. Munné-Bosch, S. and Alegre, L. (2002) Plant aging increases oxidative stress in chloroplasts. Planta, 214, 608-615.
28. Neuhaus, H.E. and Emes, M.J. (2000) Nonphotosynthetic metabolism in plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 111-140.
29. Ni, W., Robertson, E.F. and Reeves, H.C. (1987) Purification and characterisation of cytosolic NADP specific isocitrate dehydrogenase from Pisum sativum. Plant Physiol. 83, 785-788.
30. Noctor, G. and Foyer, C.H. (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 249-279.
31. Orvar, B.L. and Ellis, B.E. (1997) Transgenic tobacco plants expressing antisense RNA for cytosolic ascorbate peroxidase show increased susceptibility to ozone injury. Plant J. 11, 1297-1305.
32. 2 and antioxidants between the bundle sheath and mesophyll cells of maize leaves. J. Exp. Bot. 51, 107-113.
33. Russell, R.L., Siedlak, S.L., Raina, A.K. and Bautista, J.M. (1999) Increased neuronal glucose 6-phosphate dehydrogenase and sulfhydryl levels indicate reductive compensation to oxidative stress in Alzheimer's disease. Arch. Biochem. Biophys. 370, 236-239.
34. Salvemini, F., Franze, A., Iervolino, A., Filosa, S., Salzano, S. and Ursini, M.V. (1999) Enhanced levels and oxidoresistance mediated by increased glucose 6-phosphate dehydrogenase. J. Biol. Chem. 274, 2750-2757.
35. Sambrook, J., Fritsch, E.F. and Maniatis, P.J. (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
36. Scandalios, J.G. (1993) Oxygen stress and superoxide dismutases. Plant Physiol. 101, 7-12.
37. Scheibe, R. and Anderson, L.E. (1981) Dark modulation of NADP-dependent malate dehydrogenase and glucose 6-phosphate dehydrogenase in the chloroplast. Biochim. Biophys. Acta, 636, 58-64.
38. Shen, W.J. and Forde, B.G. (1989) Efficient transformation of Agrobacterium species by high-voltage electroporation. Nucl. Acids Res. 17, 8385.
39. Smirnoff, N. (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol. 126, 419-448.
40. Tetlow, I.J., Blissett, K.J. and Emes, M.J. (1998) Metabolite pools during starch synthesis and carbohydrate oxidation in amyloplasts isolated from wheat endosperm. Planta, 204, 100-108.
41. Tetlow, I.J., Bowsher, C.G. and Emes, M.J. (2003) Biochemical properties and enzymic capacities of chromoplasts isolated from wild buttercup (Ranunculus acris L.). Plant Sci. 165, 383-394.
42. Tiessen, A., Hendriks, J.H.M., Stitt, M., Branscheid, A., Gibon, Y., Faràe, E.M. and Geigenberger, P. (2002) Starch synthesis in potato tubers is regulated by post-translational modification of ADP-glucose pyrophosphorylase. Plant Cell, 14, 2191-2213.
43. Wendt, U.K., Hauschild, R., Lange, C., Pietersma, M., Wenderoth, I. and von Schaewen, A. (1999) Evidence for functional convergence of redox regulation in G6PDH isoforms of cyanobacteria and higher plants. Plant Mol. Biol. 40, 487-494.
44. Wendt, U.K., Wenderoth, I., Tegeler, A. and von Schaewen, A. (2000) Molecular characterization of a novel glucose-6-phosphate dehydrogenase from potato (Solanum tuberosum L.). Plant J. 23, 723-733.