Ascorbic acid: Metabolism and functions of a multi-facetted molecule

Current Opinion in Plant Biology

Volumn 3, Issue 3, 2000, Pages 229-235

  Smirnoff, Nicholas ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA;

EID: 0034103729     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5266(00)00069-8     Document Type: Review

References (55)

1. shc adaptor protein controls oxidative stress response and life span in mammals. Nature. 402:1999;309-313.
2. Shintani D., DellaPenna D. Elevating the vitamin E content of plants through metabolic engineering. Science. 282:1998;2098-2100.
3. Cobbett C.S. Phytochelatin biosynthesis and function in heavy metal detoxification. Curr Opin Plant Biol. 3:2000;211-216.
4. Noctor G., Foyer C.H. Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol. 49:1998;249-279.
5. Asada K. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Ann Rev Plant Physiol Plant Mol Biol. 50:1999;601-639.
6. Smirnoff N. The function and metabolism of ascorbic acid in plants. Ann Botany. 78:1996;661-669.
7. Horemans N., Asard H., Caubergs R.J. The role of ascorbate free radical as an electron acceptor to cytochrome b-mediated trans-plasma membrane electron transport in higher plants. Plant Physiol. 104:1994;1455-1458.
8. Horemans N., Asard H., Caubergs R.J. Carrier mediated uptake of dehydroascorbate into higher plant plasma membrane vesicles shows trans-stimulation. FEBS Lett. 421:1998;41-44.
9. Berczi A., Moller I.M. NADH-monodehydropascorbate oxidoreductase is one of the redox enzymes in spinach leaf plasma membranes. Plant Physiol. 116:1998;1029-1036.
10. Wheeler G.L., Jones M.A., Smirnoff N. The biosynthetic pathway of vitamin C in higher plants. Nature. 393:1998;365-369.
11. Smirnoff N., Wheeler G.L. Ascorbic acid metabolism in plants. Bryant J.A., Burrell M.M., Kruger N.J. Plant Carbohydrate Biochemistry. 1999;215-229 Bios Scientific Publishers, Oxford.
12. Loewus F.A. Biosynthesis and metabolism of ascorbic acid in plants and of analogs of ascorbic acid in fungi. Phytochem. 52:1999;193-210. A concise but comprehensive review of ascorbate biosynthesis and catabolism providing an assessment of the current ideas about biosynthesis, alternative pathways and a historical perspective.
13. Conklin P.L., Pallanca J.E., Last R.L., Smirnoff N. L-Ascorbic acid metabolism in the ascorbate-deficient Arabidopsis mutant vtc1. Plant Physiol. 115:1997;1277-1285.
14. ••], provides genetic evidence of the proposed [10] involvement of GDP-mannose in ascorbate biosynthesis. The enzyme catalyses the formation of GDP-mannose from mannose-1-phosphate and GTP. The gene encoding the vtc1 mutation of A. thaliana, which causes ascorbate deficiency, was cloned and found to have homology with GDP-mannose pyrophosphorylase. Vtc1 leaves had lower GDP-mannose pyrophosphorylase activity than the wild-type, and expression of wild-type VTC1 in the mutant plants restored ascorbate concentration. Reduced GDP-mannose pyrophosphorylase activity is caused by a point mutation that reduces enzyme-specific activity; transcript levels are unaffected in the mutant.
15. ••], provides genetic evidence of the involvement of GDP-mannose in ascorbate biosynthesis. GDP-mannose pyrophosphorylase was cloned from potato using an A. thaliana expressed sequence tag. Antisense expression of this gene in potato resulted in plants with reduced ascorbate concentration. GDP-mannose pyrophosphorylase appears to control ascorbate biosynthesis pathway flux because there is a close correlation between reduction in activity of this enzyme and ascorbate content. The mannose and galactose content of cell wall polysaccharides was also reduced in leaves, as would be expected if GDP-mannose and GDP-L-galactose are precursors of hemicelluloses. The antisense plants also showed necrotic leaf and stem lesions, and accelerated leaf senescence. It is not known if these symptoms are caused by ascorbate deficiency or altered cell wall composition.
16. Pego J.V., Weisbeck P.J., Smeekens S.C.M. Mannose inhibits Arabidopsis germination via a hexokinase-mediated step. Plant Physiol. 119:1999;1017-1023.
17. Stein J.C., Hansen G. Mannose induces an endonuclease responsible for DNA laddering in plants. Plant Physiol. 121:1999;71-79.
18. Østergaard J., Persiau G., Cavey M.W., Bauw G., Van Montagu M. Isolation and cDNA cloning for L-galactono-γ-lactone dehydrogenase, an enzyme involved in the biosynthesis of ascorbic acid in plants. J Biol Chem. 272:1997;30009-30016.
19. Imai T., Karita S., Shatori G., Hattori M., Nunome T., Oba K., Hirai M. L-Galactono-γ-lactone dehydrogenase from sweet potato: purification and cDNA sequence analysis. Plant Cell Physiol. 39:1998;1350-1358.
20. Siendones E., González-Reyes J.A., Santos-Ocaña C., Navas P., Córdoba F. Biosynthesis of ascorbic acid in kidney bean. L-galactono-γ-lactone dehydrogenase is an intrinsic protein located at the mitochondrial inner membrane. Plant Physiol. 120:1999;907-912. L-galactono-1,4-lactone dehydrogenase is the last enzyme in the ascorbate biosynthesis pathway and its association with the mitochondria has been recognised for some time. This paper uses purified Phaseolus vulgaris mitochondria to show that the enzyme is located in the inner mitochondrial membrane. This finding raises the possibility that ascorbate biosynthesis could be controlled through a link to mitochondrial, and therefore chloroplastic, metabolism.
21. •] cause small but detectable increases in ascorbate. The results suggest that alternative pathways involving uronic acid intermediates could make a small contribution to ascorbate synthesis.
22. •] in which D-glucosone and L-sorbosone are proposed as ascorbate precursors. Isotope-dilution experiments show that sorbosone is not involved in ascorbate synthesis. No evidence for glucosone synthesis was found and exogenous glucosone was toxic to pea seedlings. There was a close relationship between the appearance of ascorbate and ascorbate oxidase activity; both are almost absent until 20 h after imbibing the seeds, and the start of embryonic axis growth. These results are further circumstantial evidence of the role of ascorbate and ascorbate oxidase in cell growth.
23. Smirnoff N., Pallanca J.E. Ascorbate metabolism in relation to oxidative stress. Biochem Soc Trans. 24:1996;472-478.
24. Grace S.C., Logan B.A. Acclimation of foliar antioxidant systems to growth irradiance in three broadleaved evergreen species. Plant Physiol. 112:1996;1631-1640.
25. Eskling M., Akerlund H.E. Changes in the quantities of violaxanthin de-epoxidase, xanthophylls and ascorbate in spinach upon shift from low to high light. Photosynth Res. 57:1998;41-50.
26. 14C-ascorbate. The rate of ascorbate turnover is directly proportional to its pool size.
27. 14C-oxalate, showing it is not a dead-end product.
28. Ishikawa T., Yoshimura K., Sakai K., Tamoi M., Takeda T., Shigeoka S. Molecular characterization and physiological role of a glyoxysome-bound ascorbate peroxidase from spinach. Plant Cell Physiol. 39:1998;23-34.
29. Foyer C.H., Noctor G. Leaves in the dark see in the light. Science. 284:1999;599-601.
30. Niyogi K.K. Photoprotection revisited: genetic and molecular approaches. Ann Rev Plant Physiol Plant Mol Biol. 50:1999;333-359.
31. Karpinski S., Escobar C., Karpinska B., Creissen G., Mullineaux P.M. Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light. Plant Cell. 9:1997;627-640.
32. 2 is suggested as a component of the signalling system.
33. Pfannschmidt T., Nilsson A., Allen J.F. Photosynthetic control of chloroplast gene expression. Nature. 397:1999;625-628.
34. ••] do not show that increased APX transcript level is associated with more protein or enzyme activity; in some circumstances [37] this is not the case.
35. Tsugane K., Kobayashi K., Niwa Y., Ohba Y., Wada K., Kobayshi H. A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell. 11:1999;1195-1206. An A. thaliana mutant that could be affected in a signalling pathway for oxidative stress is identified. The recessive mutant (pst1) is more resistant to salt stress in high light. This treatment causes photo-oxidation, eventually resulting in bleaching of the cotyledons. APX and superoxide dismutase activity are induced by salt treatment. These enzymes have higher activity in the mutant and, notably in the case of APX, the salt-induced increase in activity is greater in the mutant than in wild-type plants. The results, although preliminary, indicate that the gene encoding this mutation could be involved in signalling oxidative stress.
36. Takahashi H., Chen Z., Du H., Liu Y., Klessig D.F. Development of necrosis and activation of disease resistance in tobacco plants with severely reduced catalase levels. Plant J. 11:1997;993-1005.
37. Mittler R., Feng X.Q., Cohen M. Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco. Plant Cell. 10:1998;461-473.
38. ••]; the treatment period was much longer than that described in other papers. The results indicate that APX expression and activity are controlled in a complex manner when plants are responding to pathogen attack.
39. Vanacker H., Carver T.L.W., Foyer C.H. Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol. 117:1998;1103-1114.
40. Wendehenne D., Durner J., Chen Z.X., Klessig D.F. Benzothiadiazole, an inducer of plant defenses, inhibits catalase and ascorbate peroxidase. Phytochem. 47:1998;651-657.
41. Hideg E., Mano J., Ohno C., Asada K. Increased levels of monodehydroascorbate radical in UV-B-irradiated broad bean leaves. Plant Cell Physiol. 38:1997;684-690.
42. Conklin P.L., Williams E.H., Last R.L. Environmental stress tolerance of an ascorbic acid-deficient Arabidopsis mutant. Proc Natl Acad Sci USA. 93:1996;9970-9974.
43. Moldau H., Bichele I., Huve K. Dark-induced ascorbate deficiency in leaf cell walls increases plasmalemma injury under ozone. Planta. 207:1998;60-66.
44. Jakob B., Heber U. Apoplastic ascorbate does not prevent the oxidation of fluorescent amphiphilic dyes by ambient and elevated concentrations of ozone in leaves. Plant Physiol Biochem. 36:1998;313-322.
45. Orvar B.L., Ellis B.E. Transgenic tobacco plants expressing antisense RNA for cytosolic ascorbate peroxidase show increased susceptibility to ozone injury. Plant J. 11:1997;1297-1305.
46. 2 in the chloroplasts and mitochondria, than wild-type plants.
47. Eskling M., Arvidsson P-O., Åkerlund H-E. The xanthophyll cycle, its regulation and components. Physiol Plant. 100:1997;806-816.
48. 1. These results provide further evidence of a relationship between apoplastic AO and cell expansion, and suggest that AO expression levels vary through the cell cycle.
49. Kisu Y., Harada Y., Goto M., Esaka M. Cloning of the pumpkin ascorbate oxidase gene and analysis of a cis-acting region involved in induction by auxin. Plant Cell Physiol. 38:1997;631-637.
50. Gonzales-Reyes J.A., Hidalgo A., Caler J.A., Palos R., Navas P. Nutrient uptake changes in ascorbate free radical-stimulated roots. Plant Physiol. 104:1994;271-276.
51. Gonzalez-Reyes J.A., Alcain F.J., Caler J.A., Serrano A., Cordoba F., Navas P. Stimulation of onion root elongation by ascorbate and ascorbate free radical in Allium cepa L. Protoplasma. 184:1995;31-35.
52. Sommer-Knudsen J., Bacic A., Clarke A.E. Hydroxyproline-rich plant glycoproteins. Phytochem. 47:1998;483-497.
53. De Gara L., Tommasi F., Liso R., Arrigoni O. Ascorbic acid utilization by prolyl hydroxylase in vivo. Phytochem. 30:1991;1397-1399.
54. De Tullio M.C., Paciolla C., Dalla Vechia F., Rascio N., D'Emerico S., De Gara L., Liso R., Arrigoni O. Changes in onion root development induced by the inhibition of peptidyl-prolyl hydroxylase and influence of the ascorbate system on cell division and elongation. Planta. 209:1999;424-434. Ascorbate is a cofactor for a number of enzymes, particularly dioxygenases, in which it maintains the reduced form of the Fe cofactor. These include enzymes involved in ethylene (e.g. ACC [1-aminocyclopropane-1-carboxylic acid] oxidase) and gibberellin synthesis. Prolyl hydroxylase, is an ascorbate-dependent enzyme that hydroxylates prolyl residues that occur in proteins such as the HRGPs. HRGPs are cell-wall structural proteins; they are probably important in assembly of the wall and may provide defence by becoming oxidatively cross-linked in response to wounding or pathogen attack. Cross-linking increases the wall strength and impedes invasion by pathogens. This paper provides evidence of a link between ascorbate and cell division via its role in proline hydroxylation. Treatment of onion roots with 3,4-DL-dehydroproline, a prolyl hydroxylase inhibitor, causes disruption to newly-formed walls and excessive expansion of cells in the elongation zone. At the same time, ascorbate concentration increases, showing that its use by prolyl hydroxylase is a major function in meristems. It is suggested that disruption of wall synthesis results in reduced cell division. It is interesting to recall that scurvy, a disease caused by ascorbate deficiency in mammals, results from reduced synthesis of collagen, an extracellular matrix hydroxy-proline-rich protein.
55. Conklin P.L., Saracco S.A., Norris S.R., Last R.L. Identification of ascorbic acid-deficient Arabidopsis thaliana mutants. Genetics. 154:2000;847-856.