European Biophysics Journal

, Volume 37, Issue 7, pp 1241–1246 | Cite as

Role of fructose in the adaptation of plants to cold-induced oxidative stress

  • J. Bogdanović
  • M. Mojović
  • N. Milosavić
  • A. Mitrović
  • Ž. Vučinić
  • I. Spasojević
Original Paper


This work presents findings, which indicate important role of fructose, fructose 6-phosphate (F6P), and fructose 1,6-bisphosphate (FBP) in preservation of homeostasis in plants under low temperature. Cold combined with light is known to incite increased generation of superoxide in chloroplasts leading to photoinhibition, but also an increased level of soluble sugars. In the present study, oxidative stress in pea leaves provoked by cold/light regime was asserted by the observed decrease of the level of oxidized form of PSI pigment P700 (P700+). Alongside, the increased antioxidative status and the accumulation of fructose were observed. The antioxidative properties of fructose and its phosphorylated forms were evaluated to appraise their potential protective role in plants exposed to chilling stress. Fructose, and particularly F6P and FBP exhibited high capacities for scavenging superoxide and showed to be involved in antioxidative protection in pea leaves. These results combined with previously established links implicate that the increase in level of fructose sugars through various pathways intercalated into physiological mechanisms of homeostasis represents important non-enzymatic antioxidative defense in plants under cold-related stress.


Fructose Oxidative stress Superoxide Low temperature Photoinhibition 



Fructose 6-phosphate


Fructose 1,6-bisphosphate


Reactive oxygen species


Oxidative pentose-phosphate pathway


Photosystem I


Superoxide dismutase


2,2′-Azino-bis(3-ethylbenzthiazoline-6-sulphonic acid)



We are grateful to Mihajlo B. Spasić for constructive discussion. This work was supported by the Grants from the Ministry of Science of Republic of Serbia, 143016 and 143043.


  1. Andjus RK (1964) Proceedings of the first international symposium on basic environmental problems of man in space. Springer, Vienna, pp 105–131Google Scholar
  2. Aver’yanov AA, Lapikova VP (1989) Interaction of sugars and hydroxyl radicals as related to antifungal toxicity of leaf secretions. Biochem Engl Transl 54:1646–1651Google Scholar
  3. Blagojević DP (2007) Antioxidant systems in supporting environmental and programmed adaptations to low temperature. Cryolett 28:137–150Google Scholar
  4. Cano A, Hernández-Ruiz J, Garcia-Cánovas F, Acosta M, Arnao MB (1998) An end-point method for estimation of the total antioxidant activity in plant material. Phytochem Anal 9:196–202CrossRefGoogle Scholar
  5. Ciereszko I, Johansson H, Kleczkowski LA (2001) Sucrose and light regulation of a cold-inducible UDP-glucose pyrophosphorylase gene via a hexokinase-independent and abscisic acid-insensitive pathway in Arabidopsis. Biochem J 354:67–72CrossRefGoogle Scholar
  6. Couée I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459CrossRefGoogle Scholar
  7. Crecelius F, Streb P, Feierabend J (2003) Malate metabolism and reactions of oxidoreduction in cold-hardened winter rye (Secale cereale L.) leaves. J Exp Bot 54:1075–1083CrossRefGoogle Scholar
  8. Deryabin AN, Dubinina IM, Burakhanova EA, Astakhova NV, Sabel’nikova EP, Trunova TI (2005) Influence of yeast-derived invertase gene expression in potato plants on membrane lipid peroxidation at low temperature. J Therm Biol 30:73–77CrossRefGoogle Scholar
  9. Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plant 92:696–717CrossRefGoogle Scholar
  10. Foyer CH, Vanacker H, Gomez LD, Harbinson J (2002) Regulation of photosynthesis and antioxidant metabolism in maize leaves at optimal and chilling temperatures: review. Plant Physiol Biochem 40:659–668CrossRefGoogle Scholar
  11. Girard A, Madani S, El Boustani ES, Belleville J, Prost J (2005) Changes in lipid metabolism and antioxidant defense status in spontaneously hypertensive rats and Wistar rats fed a diet enriched with fructose and saturated fatty acids. Nutrition 21:240–248CrossRefGoogle Scholar
  12. Havaux M, Davaud A (1994) Photoinhibition of photosynthesis in chilled potato leaves with a loss of photosystem-II activity preferential inactivation of photosystem I is not correlated. Photosynth Res 40:75–92CrossRefGoogle Scholar
  13. Hodgson RAJ, Raison JK (1991) Superoxide production by thylakoids during chilling and its implication in the susceptibility of plants to chilling-induced photoinhibition. Planta 183:222–228CrossRefGoogle Scholar
  14. Inoue K, Sakurai H, Hiyama T (1986) Photoinactivation sites of photosystem I in isolated chloroplasts. Plant Cell Phys 27:961–968Google Scholar
  15. Ivanov AG, Morgan RM, Gray GR, Velitchova MY, Huner NPA (1998) Temperature/light dependent development of selective resistance of photoinhibition of photosystem I. FEBS Lett 430:288–292CrossRefGoogle Scholar
  16. Lazzarino G, Viola AR, Mulieri L, Rotilio G, Mavelli I (1987) Prevention by fructose-1,6-bis phosphate of cardiac oxidative damage induced in mice by subchronic doxorubicin treatment. Cancer Res 47:6511–6516Google Scholar
  17. Levitt J (1980) Responses of plants to environmental stresses. Chilling, freezing and high temperature stresses vol 1. Academic Press, New YorkGoogle Scholar
  18. Maciejewska U, Bogatek R (2002) Glucose catabolism in leaves of cold-treated winter rape plants. J Plant Physiol 159:397–402CrossRefGoogle Scholar
  19. Maksimović V, Mojović M, Vučinić Ž (2006) Monosaccharide–H2O2 reactions as a source of glycolate and their stimulation by hydroxyl radicals. Carbohydr Res 341:2360–2369CrossRefGoogle Scholar
  20. McCord JM, Fridovich J (1968) The reduction of cytochrome c by milk xanthine oxidase. J Biol Chem 243:5753–5760Google Scholar
  21. Pastori G, Foyer CH, Mullineaux P (2000) Low-temperature induced changes in the distribution of H2O2 and antioxidants in the bundle sheath and mesophyll cells of maize leaves. J Exp Bot 51:107–113CrossRefGoogle Scholar
  22. Sassenrath GF, Ort DR, Portis AR (1990) Impaired reductive activation of stromal bisphosphatases in tomato leaves following low-temperature exposure at high light. Arch Biochem Biophys 282:302–308CrossRefGoogle Scholar
  23. Sonoike K (1995) Selective photoinhibition of photosystem I in isolated thylakoid membranes from cucumber and spinach. Plant Cell Physiol 36:825–830Google Scholar
  24. Sonoike K (1996) Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol 37:239–247Google Scholar
  25. Sonoike K, Terashima I, Iwaki M, Itoh S (1995) Destruction of photosystem I iron-sulfur centers in leaves of Cucumis sativus L. by weak illumination at chilling temperatures. FEBS Lett 362:235 238CrossRefGoogle Scholar
  26. Streb P, Aubert S, Gout E, Bligny R (2003) Cold- and light-induced changes of metabolite and antioxidant levels in two high mountain plant species Soldanella alpina and Ranunculus glacialis and a lowland species Pisum sativum. Physiol Plant 118:96–104CrossRefGoogle Scholar
  27. Tjus SE, Møller BL, Scheller HV (1998) Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. Plant Physiol 116:755–764CrossRefGoogle Scholar
  28. Terashima I, Funayama S, Sonoike K (1994) The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II. Planta 193:300–306CrossRefGoogle Scholar
  29. Van Breusegem F, Slooten L, Stassart JM, Botterman J, Moens T, Van Montagu M, Inze D (1999) Effects of overproduction of tobacco MnSOD in maize chloroplasts on foliar tolerance to cold and oxidative stress. J Exp Bot 50:71–78CrossRefGoogle Scholar
  30. Wise RR (1995) Chilling-enhanced photooxidation: the production, action and study of reactive oxygen species produced during chilling in the light. Photosynth Res 45:79–97CrossRefGoogle Scholar

Copyright information

© EBSA 2008

Authors and Affiliations

  • J. Bogdanović
    • 1
  • M. Mojović
    • 2
  • N. Milosavić
    • 3
  • A. Mitrović
    • 1
  • Ž. Vučinić
    • 1
  • I. Spasojević
    • 1
  1. 1.Institute for Multidisciplinary ResearchBelgradeSerbia
  2. 2.Faculty for Physical ChemistryUniversity of BelgradeBelgradeSerbia
  3. 3.Department of ChemistryInstitute of Chemistry, Technology, and MetallurgyBelgradeSerbia

Personalised recommendations