Skip to main content
Log in

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

  • Original Paper
  • Published:
European Biophysics Journal Aims and scope Submit manuscript


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.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others



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)


  • Andjus RK (1964) Proceedings of the first international symposium on basic environmental problems of man in space. Springer, Vienna, pp 105–131

    Google Scholar 

  • Aver’yanov AA, Lapikova VP (1989) Interaction of sugars and hydroxyl radicals as related to antifungal toxicity of leaf secretions. Biochem Engl Transl 54:1646–1651

    Google Scholar 

  • Blagojević DP (2007) Antioxidant systems in supporting environmental and programmed adaptations to low temperature. Cryolett 28:137–150

    Google Scholar 

  • 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 9:196–202

    Article  Google Scholar 

  • 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 354:67–72

    Article  Google Scholar 

  • 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 57:449–459

    Article  Google Scholar 

  • 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 54:1075–1083

    Article  Google Scholar 

  • 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 30:73–77

    Article  Google Scholar 

  • Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plant 92:696–717

    Article  Google Scholar 

  • 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 40:659–668

    Article  Google Scholar 

  • 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 21:240–248

    Article  Google Scholar 

  • 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 40:75–92

    Article  Google Scholar 

  • Hodgson RAJ, Raison JK (1991) Superoxide production by thylakoids during chilling and its implication in the susceptibility of plants to chilling-induced photoinhibition. Planta 183:222–228

    Article  Google Scholar 

  • Inoue K, Sakurai H, Hiyama T (1986) Photoinactivation sites of photosystem I in isolated chloroplasts. Plant Cell Phys 27:961–968

    Google Scholar 

  • 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 430:288–292

    Article  Google Scholar 

  • 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 47:6511–6516

    Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stresses. Chilling, freezing and high temperature stresses vol 1. Academic Press, New York

    Google Scholar 

  • Maciejewska U, Bogatek R (2002) Glucose catabolism in leaves of cold-treated winter rape plants. J Plant Physiol 159:397–402

    Article  Google Scholar 

  • Maksimović V, Mojović M, Vučinić Ž (2006) Monosaccharide–H2O2 reactions as a source of glycolate and their stimulation by hydroxyl radicals. Carbohydr Res 341:2360–2369

    Article  Google Scholar 

  • McCord JM, Fridovich J (1968) The reduction of cytochrome c by milk xanthine oxidase. J Biol Chem 243:5753–5760

    Google Scholar 

  • 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 51:107–113

    Article  Google Scholar 

  • 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 282:302–308

    Article  Google Scholar 

  • Sonoike K (1995) Selective photoinhibition of photosystem I in isolated thylakoid membranes from cucumber and spinach. Plant Cell Physiol 36:825–830

    Google Scholar 

  • Sonoike K (1996) Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol 37:239–247

    Google Scholar 

  • 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 362:235 238

    Article  Google Scholar 

  • 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 118:96–104

    Article  Google Scholar 

  • Tjus SE, Møller BL, Scheller HV (1998) Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. Plant Physiol 116:755–764

    Article  Google Scholar 

  • 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 193:300–306

    Article  Google Scholar 

  • 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 50:71–78

    Article  Google Scholar 

  • Wise RR (1995) Chilling-enhanced photooxidation: the production, action and study of reactive oxygen species produced during chilling in the light. Photosynth Res 45:79–97

    Article  Google Scholar 

Download references


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.

Author information

Authors and Affiliations


Corresponding author

Correspondence to I. Spasojević.

Additional information

Regional Biophysics conference of the National Biophysical Societies of Austria, Croatia, Hungary, Italy, Serbia, and Slovenia.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bogdanović, J., Mojović, M., Milosavić, N. et al. Role of fructose in the adaptation of plants to cold-induced oxidative stress. Eur Biophys J 37, 1241–1246 (2008).

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: