Skip to main content
Log in

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

Planta Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

Glc6P:

glucose-6-phosphate

Glc1P:

glucose-1-phosphate

Fru6P:

fructose-6-phosphate

PPi :

inorganic pyro-phosphate

References

  • 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 1–29

    Google Scholar 

  • 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 1–42

    Google Scholar 

  • ap Rees T, Hill SA (1994) Metabolic control analysis of plant metabolism. Plant Cell Environ 17: 587–599

    Google Scholar 

  • 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 227–238

    Google Scholar 

  • Ball KL, ap Rees T (1988) Frutose 2,6-bisphosphate and the climacteric in bananas. Eur J Biochem 177: 637–641

    Google Scholar 

  • Ball KL, Green JH, ap Rees T (1991) Glycolysis at the climacteric of bananas. Eur J Biochem 197: 265–269

    Google Scholar 

  • Banks NH (1983) Evaluation of methods for determining internal gases in banana fruit. J Exp Bot 34: 871–879

    Google Scholar 

  • 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: 577–596

    Google Scholar 

  • Barman TE (1969) The enzyme handbook. Springer-Verlag, Berlin, Germany

    Google Scholar 

  • 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: 321–325

    Google Scholar 

  • 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, 107–128

    Google Scholar 

  • Dixon WL, ap Rees T (1980) Identification of the regulatory steps in glycolysis in potato tubers. Phytochemistry 19: 1297–1301

    Google Scholar 

  • Effer WF, Ranson SL (1967) Some effects of oxygen concentration on levels of respiratory intermediates in buckwheat seedlings. Plant Physiol 42: 1053–1058

    Google Scholar 

  • Faiz-ur-Rahman ATM, Trewavas AJ, Davies DD (1974) The Pasteur effect in carrot root tissue. Planta 118: 195–210

    Google Scholar 

  • 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: 81–90

    CAS  Google Scholar 

  • 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: 198–204

    Google Scholar 

  • 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: 29–33

    Google Scholar 

  • Hill SA, ap Rees T (1994) Fluxes of carbohydrate metabolism in ripening bananas. Planta 192: 52–60

    Google Scholar 

  • Hill SA, ap Rees T (1995) The effect of glucose on the control of carbohydrate metabolism in ripening bananas. Planta 196: 335–343

    CAS  Google Scholar 

  • Jenkin LET, ap Rees T (1986) Effects of lack of oxygen on the metabolism of shoots of Typha angustifolia. Phytochemistry 25: 823–827

    Google Scholar 

  • 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: 251–258

    Google Scholar 

  • Kobr MJ, Beevers H (1971) Gluconeogenesis in castor bean endosperm. Changes in glycolytic intermediates. Plant Physiol 47: 48–52

    Google Scholar 

  • Kruger NJ, ap Rees T (1983) Properties of α-glucan phosphorylase from pea chloroplasts. Phytochemistry 22: 1891–1898

    Google Scholar 

  • Leshuk JA, Saltveit ME (1991) Effects of rapid changes in oxygen concentration on the respiration of carrot roots. Physiol Plant 82: 559–568

    Google Scholar 

  • 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: 5540–5544

    Google Scholar 

  • Mertens E (1991) Pyrophosphate-dependent phosphofructokinase, an anaerobic glycolytic enzyme? FEBS Lett 285: 1–5

    Google Scholar 

  • Mertens E, Larondelle Y, Hers H-G (1990) Induction of pyrophosphate: fructose-6-phosphate 1-phosphotransferase by anoxia in rice seedlings. Plant Physiol 93: 584–587

    Google Scholar 

  • 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: 75–82

    Google Scholar 

  • 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: 189–193

    Google Scholar 

  • Preiss J (1988) Biosynthesis of starch and its regulation. In: Preiss J (ed) Biochemistry of plants, vol. 14. Academic Press, London, UK, pp 181–254

    Google Scholar 

  • 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: 480–488

    CAS  Google Scholar 

  • Renz A, Stitt M (1993) Substrate specificity and product inhibition of different forma of fructokinases and hexokinases in developing potato tubers. Planta 190: 166–175

    Google Scholar 

  • 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: 893–902

    Google Scholar 

  • Smith AM, ap Rees T (1979) Effects of anaerobiosis on carbohydrate oxidation by roots of Pisum, sativum. Phytochemistry 18: 1453–1458

    Google Scholar 

  • Stitt M (1989) Product inhibition of potato tuber pyrophosphate: fructose-6-phosphate phosphotransferase by phosphate and pyrophosphate. Plant Physiol 89: 628–633

    Google Scholar 

  • Stitt M (1990) Fructose-2,6-bisphosphate as a regulatory molecule in plants. Annu Rev Plant Physiol Plant Mol Biol 41: 153–185

    Google Scholar 

  • Stitt M, Lilley RMcC, Heldt HW (1982) Adenine nucleotide levels in the cytosol, chloroplasts, and mitochondria of wheat leaf protoplasts. Plant Physiol 70: 971–977

    Google Scholar 

  • Stryer L (1981) Biochemistry, WH Freeman and Co., San Francisco, USA

    Google Scholar 

  • Theodorou ME, Plaxton WC (1994) Induction of PPi-dependent phosphofructokinase by phosphate starvation in seedlings of Brassica nigra. Plant Cell Environ 17: 287–294

    Google Scholar 

  • Thomas S, Kruger NJ (1994) Source of apparent ADP-dependent phosphofructokinase activity in plants extracs. Plant Sci 95: 133–139

    Google Scholar 

  • 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: 31–39

    Google Scholar 

  • Winter H, Robinson DG, Heldt HW (1994) Subcellular volumes and metabolite concentrations in spinach leaves. Planta 193:530–535

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

We thank Geest Foods Group, Great Dunmow, Essex, UK for giving us the bananas. S.A.H. thanks the managers of the Brood bank Fund for a fellowship.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hill, S.A., ap Rees, T. The effect of hypoxia on the control of carbohydrate metabolism in ripening bananas. Planta 197, 313–323 (1995). https://doi.org/10.1007/BF00202653

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00202653

Keywords

Navigation