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Planta

, Volume 197, Issue 2, pp 313–323 | Cite as

The effect of hypoxia on the control of carbohydrate metabolism in ripening bananas

  • Steven A Hill
  • Tom ap Rees
Article

Abstract

The aim of this work was to determine the effects of hypoxia on the major fluxes of carbohydrate metabolism in climacteric fruit of banana (Musa cavendishii Lamb ex Paxton). Hands of bananas, untreated with ethylene, were allowed to ripen in air at 21°C in the dark. When the climacteric began, fruit were transferred to 15 or 10% oxygen and were analysed once the climacteric peak had been reached 8–12 h later. The rates of starch breakdown, sucrose, glucose and fructose accumulation, and CO2 production were determined, as were the contents of hexose monophosphates, adenylates and pyruvate. In addition, the detailed distribution of label was determined after supplying [U-14C]-, [1-14C]-, [3,4-14C]- and [6-14C]glucose, and [U-14C]glycerol to cores of tissue under hypoxia. The data were used to estimate the major fluxes of carbohydrate metabolism. There was a reduction in the rate of respiration. The ATP/ADP ratio was unaffected but there was a significant increase in the content of AMP. In 15% oxygen only minor changes in fluxes were observed. In 10% oxygen starch breakdown was reduced and starch synthesis was not detected. The rate of sucrose synthesis decreased, as did the rate of re-entry of hexose sugars into the hexose monophosphate pool. There was a large increase in both the glycolytic flux and in the flux from triose phosphates to hexose monophosphates. It is argued that the increase in these fluxes is due to activation of pyrophosphate: fructose-6-phosphate 1-phosphotransferase, and that this enzyme has an important role in hypoxia. The results are discussed in relation to our understanding of the control of carbohydrate metabolism in hypoxia.

Keywords

Carbohydrate metabolism (fluxes) Hypoxia Musa (fruit ripening) Respiration Starch break-down Sucrose synthesis 

Abbreviations

Glc6P

glucose-6-phosphate

Glc1P

glucose-1-phosphate

Fru6P

fructose-6-phosphate

PPi

inorganic pyro-phosphate

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References

  1. ap Rees T (1980a) Assessment of the contributions of metabolic pathways to plant respiration. In: Davies DD (ed) Biochemistry of plants, vol. 2. Academic Press, London, pp 1–29Google Scholar
  2. ap Rees T (1980b) Integration of pathways of synthesis and degradation of hexose phosphates. In: Preiss J (ed) Biochemistry of plants, vol. 3. Academic Press, London, pp 1–42Google Scholar
  3. ap Rees T, Hill SA (1994) Metabolic control analysis of plant metabolism. Plant Cell Environ 17: 587–599Google Scholar
  4. ap Rees T, Jenkin LET, Smith AM, Wilson PM (1987) The metabolism of flood-tolerant plants. In: Crawford RMM (ed) Plant life in aquatic and amphibious habitats. Blackwell Scientific Publications, Oxford, UK, pp 227–238Google Scholar
  5. Ball KL, ap Rees T (1988) Frutose 2,6-bisphosphate and the climacteric in bananas. Eur J Biochem 177: 637–641Google Scholar
  6. Ball KL, Green JH, ap Rees T (1991) Glycolysis at the climacteric of bananas. Eur J Biochem 197: 265–269Google Scholar
  7. Banks NH (1983) Evaluation of methods for determining internal gases in banana fruit. J Exp Bot 34: 871–879Google Scholar
  8. Barker J, Khan MAA, Solomos T (1967) Studies in the respiratory and carbohydrate metabolism of plant tissues. XXI The mechanism of the Pasteur effect in peas. New Phytol 66: 577–596Google Scholar
  9. Barman TE (1969) The enzyme handbook. Springer-Verlag, Berlin, GermanyGoogle Scholar
  10. Brown GC, Hafner RP, Brand MD (1990) A ‘top-down’ approach to the determination of control coefficients in metabolic control theory. Eur J Biochem 188: 321–325Google Scholar
  11. Copeland L, Turner JF (1987) The regulation of glycolysis and the pentose phosphate pathway. In: Hatch MD, Boardman NK (eds) Biochemistry of plants, vol. 11. Academic Press, London, 107–128Google Scholar
  12. Dixon WL, ap Rees T (1980) Identification of the regulatory steps in glycolysis in potato tubers. Phytochemistry 19: 1297–1301Google Scholar
  13. Effer WF, Ranson SL (1967) Some effects of oxygen concentration on levels of respiratory intermediates in buckwheat seedlings. Plant Physiol 42: 1053–1058Google Scholar
  14. Faiz-ur-Rahman ATM, Trewavas AJ, Davies DD (1974) The Pasteur effect in carrot root tissue. Planta 118: 195–210Google Scholar
  15. Geigenberger P, Stitt M (1991) A ‘futile’ cycle of sucrose synthesis and degradation is involved in regulating partitioning between sucrose, starch and respiration in cotyledons of germinating Ricinus communis L. seedlings when phloem transport is inhibited. Planta 185: 81–90Google Scholar
  16. Hatzfeld W-D, Stitt M (1990) A study of the rate of recycling of triose phosphates in heterotrophic Chenopodium rubrum cells, potato tubers, and maize endosperm. Planta 180: 198–204Google Scholar
  17. Heineke D, Wildenberger K, Sonnewald U, Willmitzer L, Heldt HW (1994) Accumulation of hexoses in leaf vacuoles: studies with transgenic tobacco plants expressing yeast-derived invertase in the cytosol, vacuole or apoplasm. Planta 194: 29–33Google Scholar
  18. Hill SA, ap Rees T (1994) Fluxes of carbohydrate metabolism in ripening bananas. Planta 192: 52–60Google Scholar
  19. Hill SA, ap Rees T (1995) The effect of glucose on the control of carbohydrate metabolism in ripening bananas. Planta 196: 335–343Google Scholar
  20. Jenkin LET, ap Rees T (1986) Effects of lack of oxygen on the metabolism of shoots of Typha angustifolia. Phytochemistry 25: 823–827Google Scholar
  21. Kanellis AK, Solomos T, Maltoo AK (1989) Changes in sugars, enzymic activities and acid phosphatase isozyme profiles of bananas ripened in air or stored in 2.5% oxygen with or without ethylene. Plant Physiol 90: 251–258Google Scholar
  22. Kobr MJ, Beevers H (1971) Gluconeogenesis in castor bean endosperm. Changes in glycolytic intermediates. Plant Physiol 47: 48–52Google Scholar
  23. Kruger NJ, ap Rees T (1983) Properties of α-glucan phosphorylase from pea chloroplasts. Phytochemistry 22: 1891–1898Google Scholar
  24. Leshuk JA, Saltveit ME (1991) Effects of rapid changes in oxygen concentration on the respiration of carrot roots. Physiol Plant 82: 559–568Google Scholar
  25. Macdonald FD, Chou Q, Buchanan BB, Stitt M (1989) Purification and characterisation of fructose-2,6-bisphosphatase, a substrate-specific cytosolic enzyme from leaves. J Biol Chem 264: 5540–5544Google Scholar
  26. Mertens E (1991) Pyrophosphate-dependent phosphofructokinase, an anaerobic glycolytic enzyme? FEBS Lett 285: 1–5Google Scholar
  27. Mertens E, Larondelle Y, Hers H-G (1990) Induction of pyrophosphate: fructose-6-phosphate 1-phosphotransferase by anoxia in rice seedlings. Plant Physiol 93: 584–587Google Scholar
  28. Mohanty B, Wilson PM, ap Rees T (1993) Effects of anoxia on growth and carbohydrate metabolism in suspension cultures of soybean and rice. Phytochemistry 34: 75–82Google Scholar
  29. Pascal N, Dumas R, Douce R (1990) Comparison of the kinetic behaviour towards pyridine nucleotides of NAD+-linked dehydrogenases from plant mitochondria. Plant Physiol 94: 189–193Google Scholar
  30. Preiss J (1988) Biosynthesis of starch and its regulation. In: Preiss J (ed) Biochemistry of plants, vol. 14. Academic Press, London, UK, pp 181–254Google Scholar
  31. Reimholz R, Geigenberger, P Stitt M (1994) Sucrose phosphate synthase is regulated via metabolites and protein phosphorylation in potato tubers, in a manner analogous to the enzyme in leaves. Planta 192: 480–488Google Scholar
  32. Renz A, Stitt M (1993) Substrate specificity and product inhibition of different forma of fructokinases and hexokinases in developing potato tubers. Planta 190: 166–175Google Scholar
  33. Rumpho ME, Kennedy RA (1983) Activity of the pentose phosphate and glycolytic pathways during anaerobic germination of Echinochloa crus-galli (banyard grass) seeds. J Exp Bot 34: 893–902Google Scholar
  34. Smith AM, ap Rees T (1979) Effects of anaerobiosis on carbohydrate oxidation by roots of Pisum, sativum. Phytochemistry 18: 1453–1458Google Scholar
  35. Stitt M (1989) Product inhibition of potato tuber pyrophosphate: fructose-6-phosphate phosphotransferase by phosphate and pyrophosphate. Plant Physiol 89: 628–633Google Scholar
  36. Stitt M (1990) Fructose-2,6-bisphosphate as a regulatory molecule in plants. Annu Rev Plant Physiol Plant Mol Biol 41: 153–185Google Scholar
  37. Stitt M, Lilley RMcC, Heldt HW (1982) Adenine nucleotide levels in the cytosol, chloroplasts, and mitochondria of wheat leaf protoplasts. Plant Physiol 70: 971–977Google Scholar
  38. Stryer L (1981) Biochemistry, WH Freeman and Co., San Francisco, USAGoogle Scholar
  39. Theodorou ME, Plaxton WC (1994) Induction of PPi-dependent phosphofructokinase by phosphate starvation in seedlings of Brassica nigra. Plant Cell Environ 17: 287–294Google Scholar
  40. Thomas S, Kruger NJ (1994) Source of apparent ADP-dependent phosphofructokinase activity in plants extracs. Plant Sci 95: 133–139Google Scholar
  41. Wendler R, Veith R, Dancer J, Stitt M, Komor E (1990) Sucrose storage in cell suspension cultures of Saccharum sp. (sugarcane) is regulated by a cycle of synthesis and degradation. Planta 183: 31–39Google Scholar
  42. Winter H, Robinson DG, Heldt HW (1994) Subcellular volumes and metabolite concentrations in spinach leaves. Planta 193:530–535Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • Steven A Hill
    • 1
  • Tom ap Rees
    • 1
  1. 1.Department of Plant SciencesUniversity of CambridgeCambridgeUK

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