Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Superoxide production by thylakoids during chilling and its implication in the susceptibility of plants to chilling-induced photoinhibition

  • 70 Accesses

  • 55 Citations

Abstract

Factors influencing the rate of superoxide (O 2 - ) production by thylakoids were investigated to determine if increased production of the radical was related to injury induced by chilling at a moderate photon flux density (PFD). Plants used were Spinacia oleracea L., Cucumis sativus L. and Nerium oleander L. grown at either 200° C or 45° C. Superoxide production was determined by electron-spin-resonance spectroscopy of the (O 2 - )-dependent rate of oxidation of 2-ethyl-1-hydroxy-2,5,5-trimethyl-3-oxazolidine (OXANOH) to the corresponding oxazolidinoxyl radical, OXANO ·. For all plants, the steady-state rate of O 2 - production by thylakoids, incubated at 25° C and 350 μmol photon · m−2 · s−1 (moderate PFD) with added ferredoxin and NADP, was between 7.5 and 12.5 μmol · (mg chlorophyll)−1 · h−1. Incubation at 5° C and a moderate PFD, decreased the rate of O 2 - production 40% and 15% by thylakoids from S. oleracea and 20° C-grown N. oleander, chillinginsensitive plants, but increased the rate by 56% and 5% by thylakoids from C. sativus and 45° C-grown N. oleander, chilling-sensitive plants. For all plants, the addition of either ferredoxin or methyl viologen increased the rate of O 2 - -production at 25° C by 75–100%. With these electron acceptors, lowering the temperature to 5° C caused only a slight decrease in O 2 - production. In the absence of added electron acceptors, thylakoids produced O 2 - at a rate which was about 45% greater than that when ferredoxin and NADP were present. The addition of 3-(3′,4′-dichlorophenyl)-1,1-dimethylurea reduced O 2 - production under all conditions tested. The results show that the rate of O 2 - production increases in thylakoids when the rate of electron transfer to NADP is reduced. This could explain differences in the susceptibility of thylakoids from chilling-sensitive and chilling-insensitive plants to chilling at a moderate PFD, and is consistent with the proposal that O 2 - production is involved in the injury leading to the inhibition of photosynthesis induced under these conditions.

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

Abbreviations

Chl:

chlorophyll

DCMU:

3-(3′,4′-dichlorophen-yl)-1,1-dimethylurea

Fd:

ferredoxin

MV:

methyl viologen

20°oleander:

Nerium oleander grown at 20° C

45°-oleander:

N. oleander grown at 45° C

OXANOH:

2-ethyl-1-hydroxy-2,5,5-tri-methyl-3-oxazolidine

PFD:

photon flux density (photon fluence rate)

TEMED:

tetramethyl ethylenediamine

References

  1. Asada, K., Nakano, Y. (1978) Affinity for oxygen in photoreduction of molecular oxygen and scavenging of hydrogen peroxide in spinach chloroplasts. Photochem. Photobiol. 28, 917–920

  2. Asada, K., Kiso, K., Yoshikawa, K. (1974) Univalent reduction of molecular oxygen by spinach chloroplasts on illumination. J. Biol. Chem. 249, 2175–2181

  3. Asada, K., Takahashi, M-A., Hayakawa, T. (1983) Photoproduction of superoxide in membranes of chloroplasts and intrachloroplast distribution of superoxide dismutase. In: Oxy radicals and their scavenging system, vol. I, pp. 240–245, Cohen, G., Greenwald, R.A. eds. Elsevier, Amsterdam

  4. Badger, M.R. (1985) Photosynthetic oxygen exchange. Annu. Rev. Plant Physiol. 36, 27–53

  5. Elstner, E.F. (1982) Oxygen activation and oxygen toxicity. Annu. Rev. Plant Physiol. 33, 73–96

  6. Elstner, E.F. (1987) Metabolism of activated oxygen species. In: The biochemistry of plants, vol. 11, pp. 253–317, Davies, D.D., ed. Academic Press, San Diego, Cal., USA

  7. Farrington, J.A., Ebert M., Land, E.J., Fletcher, K. (1973) Bipyridylium quaternary salts and related compounds. V. Pulse radiolysis studies of the reaction of Paraquat radical with oxygen. Implications for the mode of action of bipyridyl herbicides. Biochim. Biophys. 134, 372–381

  8. Furbank, R.T., Badger, M.R. (1983) Oxygen exchange and photophosphorylation in isolated spinach thylakoids. Biochim. Biophys. Acta 723, 400–409

  9. Furbank, R.T., Badger, M.R., Osmond, C.B. (1983) Photoreduction of oxygen in mesophyll chloroplasts of C4 plants. Plant Physiol. 73, 1038–1041

  10. Garber, M.P. (1977) Effect of light and chilling temperatures on chilling sensitive and chilling resistant plants. Pretreatment of cucumber and spinach thylakoids in vivo and in vitro. Plant Physiol. 59, 981–985

  11. Havaux, M., Lannoye, R. (1984) Effects of chilling temperatures on prompt and delayed chlorophyll fluorescence in maize and barley leaves. Photosynthetica 18, 117–127

  12. Hayakawa, T., Kanematsu, S., Asada, K. (1984) Occurrence of Cu, Zn-superoxide dismutase in the intrathylakoid space of spinach chloroplasts. Plant Cell Physiol. 25, 883–889

  13. Hodgson, R.A.J., Raison, J.K. (1989) Inhibition of photosynthesis by chilling in moderate light: A comparison of plants sensitive and insensitive to chilling. Planta 178, 545–552

  14. Hodgson, R.A.J., Orr, G.R., Raison, J.K. (1987) Inhibition of photosynthesis by chilling in the light. Plant Sci. 49, 75–79

  15. Homann, P.H. (1978) Oxygen-dependent photoxidations in photosystem II of isolated chloroplasts. In: Photosynthetic oxygen evolution, pp. 195–212, Metzner, H., ed Academic Press, London

  16. Horton, P. (1985) Interactions between electron transfer and carbon assimilation. In: Photosynthetic mechanisms and the environment, pp. 135–188, Barber, J., Baker, N.R., eds. Elsevier, Amsterdam

  17. Kaiser, W.M. (1979) Reversible inhibition of the Calvin cycle and activation of oxidative pentose phosphate cycle in isolated intact chloroplasts by H2O2. Planta 145, 377–382

  18. Keana, J., Keana, S., Beetham, D. (1967) A new versitile ketone spin label. J. Am. Chem. Soc. 89, 3055–3056

  19. Marshall, M.J., Worsfold, M. (1978) Superoxide dismutase: A direct continuous linear assay using the oxygen electrode. Anal. Biochem. 86, 561–573

  20. Marsho, T.V., Behrens, P.W., Radmer, R.J. (1979) Photosynthetic oxygen reduction in isolated intact chloroplasts and cells from spinach. Plant Physiol. 64, 656–659

  21. McRae, D.G., Thompson, J.E. (1983) Senescence-dependent changes in superoxide anion production by illuminated chloroplasts from bean leaves. Plant 158, 185–193

  22. McWilliam, J.R., Ferrar, P.J. (1974) Photosynthetic adaptation of higher plants to thermal stress. Proc. R. Soc. N. Z. 12, 467–476

  23. Nolan, W.G. (1980) Effect of temperature on electron transport activities of isolated chloroplasts. Plant Physiol. 66, 234–237

  24. Nolan, W.G., Smillie, R.M. (1977) Temperature-induced changes in Hill activity of chloroplasts isolated from chilling-sensitive and chilling-resistant plants. Plant Physiol. 59, 1141–1145

  25. Öquist, G. (1987) Environmental stress and photosynthesis. In: Progress in Photosynthesis Research, vol. 4, pp. 1–10, Biggins, J., ed. Nijhoff, Dordrecht, The Netherlands

  26. Peeler, T.C., Naylor, A.W. (1988a) A comparison of the effects of chilling on leaf gas exchange in Pea (Pisum sativum L.) and cucumber (Cucumis sativus L). Plant Phyisol. 86, 143–146

  27. Peeler, T.C., Naylor, A.W. (1988b) A comparison of the effects of chilling on thylakoid electron transfer in pea (Pisum sativum L.) and cucumber (Cucumis sativus L.). Plant Physiol. 86, 147–151

  28. Powles, S.B. (1984) Photoinhibition of photosynthesis induced by visible light. Annu. Rev. Plant Physiol. 35, 15–44

  29. Raison, J.K., Brown, M.A. (1989) Sensitivity of altitudinal ecotypes of the wild tomato Lycopersicon hirsutum to chilling injury. Plant Physiol. 91, 1471–1475

  30. Robinson, J.M. (1988) Does O2 photoreduction occur within chloroplasts in vivo? Physiol. Plant. 72, 666–680

  31. Rosen, G.M., Finkelstein, E., Rauckman, E.J. (1982) A method for the detection of superoxide in biological systems. Arch. Biochem. Biophys. 215, 367–378

  32. Shneyour, A., Raison, J.K., Smillie, R.M. (1973) The effect of temperature of the rate of photosynthetic electron transfer in chloroplasts of chilling-sensitive and chilling-resistant plants. Biochim. Biophys. Acta 292, 152–161

  33. Takahashi, M.A., Asada, K. (1983) Superoxide anion permeability of phospholipid membranes and chloroplast thylakoids. Arch. Biochem. Biophys. 226, 558–566

  34. Wise, R.R., Naylor, A. W. (1987a) Chilling-enhanced photooxidation: the peroxidative destruction of lipids during chilling injury to photosynthesis and ultastructure. Plant Physiol. 83, 272–277

  35. Wise, R.R., Naylor, A.W. (1987b) Chilling-enhanced photooxidation: Evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol. 83, 278–282

Download references

Author information

Additional information

We would like to thank R.T. Furbank, R.S.B.S., Australian National University, Canberra, A.C.T., and C.B. Osmond, now of Duke University, Durham, N.C., USA, for the gift of ferredoxin, R.A.J.H. was supported by a Commonwealth Postgraduate Research Award.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hodgson, R.A.J., Raison, J.K. Superoxide production by thylakoids during chilling and its implication in the susceptibility of plants to chilling-induced photoinhibition. Planta 183, 222–228 (1991). https://doi.org/10.1007/BF00197792

Download citation

Key words

  • Chilling
  • Cucumis
  • Nerium
  • Photoinhibition of photosynthesis
  • Photosynthesis (photoinhibition, active O2)
  • Spinacia
  • Superoxide