Skip to main content
PMC home page
Plant Physiology logoLink to Plant Physiology
. 1996 Nov;112(3):1301–1313. doi: 10.1104/pp.112.3.1301

Oxidative Stress Results in Increased Sinks for Metabolic Energy during Aging and Sprouting of Potato Seed-Tubers.

GNM Kumar 1, N R Knowles 1
PMCID: PMC158058  PMID: 12226448

Abstract

Glutathione-mediated free-radical-scavenging and plasma membrane ATPase activities increase as sinks for metabolic energy with advancing tuber age. Plasma membrane ATPase activity from 19-month-old tubers was 77% higher than that from 7-month-old tubers throughout sprouting. The higher activity was not attended by an increase in the amount of ATPase per unit plasma membrane protein. Concentrations of oxidized (GSSG) and reduced glutathione more than doubled as tuber age advanced from 6 to 30 months, but the proportion of GSSG to total glutathione remained constant with age. The activity of glutathione transferase, an enzyme that catabolizes lipid-hydroperoxides, increased by 44 and 205% on a fresh weight and protein basis, respectively, as tubers aged from 6 to 30 months. Glutathione reductase activity also increased with advancing age, by 90% on a fresh weight basis and 305% on a protein basis. Older tubers had more glutathione reductase per unit of soluble and mitochondrial protein. The age-induced increase in cytosolic glutathione transferase activity was likely due to increased availability of lipid-hydroperoxides and/or a positive effector. Synthesis of glutathione requires ATP, and the increased reduction of GSSG resulting from catalysis of lipid-hydroperoxides is NADPH-dependent. Thus, increased plasma membrane ATPase and glutathione-mediated free-radical-scavenging activities likely constitute substantial sinks for ATP in older tubers prior to and during sprouting. Increased oxidative stress and loss in membrane integrity and central features of aging that undoubtedly contribute to the enhanced respiration of sprouting older tubers.

Full Text

The Full Text of this article is available as a PDF (2.9 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson M. E. Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol. 1985;113:548–555. doi: 10.1016/s0076-6879(85)13073-9. [DOI] [PubMed] [Google Scholar]
  2. Barclay L. R. The cooperative antioxidant role of glutathione with a lipid-soluble and a water-soluble antioxidant during peroxidation of liposomes initiated in the aqueous phase and in the lipid phase. J Biol Chem. 1988 Nov 5;263(31):16138–16142. [PubMed] [Google Scholar]
  3. Bartling D., Radzio R., Steiner U., Weiler E. W. A glutathione S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana. Molecular cloning and functional characterization. Eur J Biochem. 1993 Sep 1;216(2):579–586. doi: 10.1111/j.1432-1033.1993.tb18177.x. [DOI] [PubMed] [Google Scholar]
  4. Bensadoun A., Weinstein D. Assay of proteins in the presence of interfering materials. Anal Biochem. 1976 Jan;70(1):241–250. doi: 10.1016/s0003-2697(76)80064-4. [DOI] [PubMed] [Google Scholar]
  5. Bilang J., Sturm A. Cloning and characterization of a glutathione S-transferase that can be photolabeled with 5-azido-indole-3-acetic acid. Plant Physiol. 1995 Sep;109(1):253–260. doi: 10.1104/pp.109.1.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bowler C., Alliotte T., De Loose M., Van Montagu M., Inzé D. The induction of manganese superoxide dismutase in response to stress in Nicotiana plumbaginifolia. EMBO J. 1989 Jan;8(1):31–38. doi: 10.1002/j.1460-2075.1989.tb03345.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cakmak I., Marschner H. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol. 1992 Apr;98(4):1222–1227. doi: 10.1104/pp.98.4.1222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carlberg I., Mannervik B. Glutathione reductase. Methods Enzymol. 1985;113:484–490. doi: 10.1016/s0076-6879(85)13062-4. [DOI] [PubMed] [Google Scholar]
  9. Carlenor E., Persson B., Glaser E., Andersson B., Rydström J. On the presence of a nicotinamide nucleotide transhydrogenase in mitochondria from potato tuber. Plant Physiol. 1988 Oct;88(2):303–308. doi: 10.1104/pp.88.2.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dieter P., Marmé D. A Ca2+, Calmodulin-dependent NAD kinase from corn is located in the outer mitochondrial membrane. J Biol Chem. 1984 Jan 10;259(1):184–189. [PubMed] [Google Scholar]
  11. Eraso P., Gancedo C. Activation of yeast plasma membrane ATPase by acid pH during growth. FEBS Lett. 1987 Nov 16;224(1):187–192. doi: 10.1016/0014-5793(87)80445-3. [DOI] [PubMed] [Google Scholar]
  12. Fletcher B. L., Dillard C. J., Tappel A. L. Measurement of fluorescent lipid peroxidation products in biological systems and tissues. Anal Biochem. 1973 Mar;52(1):1–9. doi: 10.1016/0003-2697(73)90327-8. [DOI] [PubMed] [Google Scholar]
  13. Gallagher S. R., Leonard R. T. Effect of vanadate, molybdate, and azide on membrane-associated ATPase and soluble phosphatase activities of corn roots. Plant Physiol. 1982 Nov;70(5):1335–1340. doi: 10.1104/pp.70.5.1335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Habig W. H., Jakoby W. B. Assays for differentiation of glutathione S-transferases. Methods Enzymol. 1981;77:398–405. doi: 10.1016/s0076-6879(81)77053-8. [DOI] [PubMed] [Google Scholar]
  15. Iswari S., Palta J. P. Plasma Membrane ATPase Activity following Reversible and Irreversible Freezing Injury. Plant Physiol. 1989 Jul;90(3):1088–1095. doi: 10.1104/pp.90.3.1088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kasamo K. Mechanism for the Activation of Plasma Membrane H-ATPase from Rice (Oryza sativa L.) Culture Cells by Molecular Species of a Phospholipid. Plant Physiol. 1990 Jul;93(3):1049–1052. doi: 10.1104/pp.93.3.1049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kasamo K., Nouchi I. The Role of Phospholipids in Plasma Membrane ATPase Activity in Vigna radiata L. (Mung Bean) Roots and Hypocotyls. Plant Physiol. 1987 Feb;83(2):323–328. doi: 10.1104/pp.83.2.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lee E. H., Bennett J. H. Superoxide Dismutase: A POSSIBLE PROTECTIVE ENZYME AGAINST OZONE INJURY IN SNAP BEANS (PHASEOLUS VULGARIS L.). Plant Physiol. 1982 Jun;69(6):1444–1449. doi: 10.1104/pp.69.6.1444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Luethy M. H., Horak A., Elthon T. E. Monoclonal Antibodies to the [alpha]- and [beta]-Subunits of the Plant Mitochondrial F1-ATPase. Plant Physiol. 1993 Mar;101(3):931–937. doi: 10.1104/pp.101.3.931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mauch F., Dudler R. Differential induction of distinct glutathione-S-transferases of wheat by xenobiotics and by pathogen attack. Plant Physiol. 1993 Aug;102(4):1193–1201. doi: 10.1104/pp.102.4.1193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. May M. J., Leaver C. J. Oxidative Stimulation of Glutathione Synthesis in Arabidopsis thaliana Suspension Cultures. Plant Physiol. 1993 Oct;103(2):621–627. doi: 10.1104/pp.103.2.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McCray P. B., Gibson D. D., Fong K. L., Hornbrook K. R. Effect of glutathione peroxidase activity on lipid peroxidation in biological membranes. Biochim Biophys Acta. 1976 Jun 22;431(3):459–468. [PubMed] [Google Scholar]
  23. Mikitzel L. J., Knowles N. R. Effect of potato seed-tuber age on plant establishment and amelioration of age-linked effects with auxin. Plant Physiol. 1990 Jul;93(3):967–975. doi: 10.1104/pp.93.3.967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Palmgren M. G., Sommarin M. Lysophosphatidylcholine stimulates ATP dependent proton accumulation in isolated oat root plasma membrane vesicles. Plant Physiol. 1989 Jul;90(3):1009–1014. doi: 10.1104/pp.90.3.1009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pardo J. M., Serrano R. Structure of a plasma membrane H+-ATPase gene from the plant Arabidopsis thaliana. J Biol Chem. 1989 May 25;264(15):8557–8562. [PubMed] [Google Scholar]
  26. Rao M. V., Hale B. A., Ormrod D. P. Amelioration of Ozone-Induced Oxidative Damage in Wheat Plants Grown under High Carbon Dioxide (Role of Antioxidant Enzymes). Plant Physiol. 1995 Oct;109(2):421–432. doi: 10.1104/pp.109.2.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Serrano R. In vivo glucose activation of the yeast plasma membrane ATPase. FEBS Lett. 1983 May 30;156(1):11–14. doi: 10.1016/0014-5793(83)80237-3. [DOI] [PubMed] [Google Scholar]
  28. Serrano R., Kanner B. I., Racker E. Purification and properties of the proton-translocating adenosine triphosphatase complex of bovine heart mitochondria. J Biol Chem. 1976 Apr 25;251(8):2453–2461. [PubMed] [Google Scholar]
  29. Smith I. K. Stimulation of glutathione synthesis in photorespiring plants by catalase inhibitors. Plant Physiol. 1985 Dec;79(4):1044–1047. doi: 10.1104/pp.79.4.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wade M. G., Van der Kraak G., Gerrits M. F., Ballantyne J. S. Release and steroidogenic actions of polyunsaturated fatty acids in the goldfish testis. Biol Reprod. 1994 Jul;51(1):131–139. doi: 10.1095/biolreprod51.1.131. [DOI] [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES