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

The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II


Maximum quantum yields (QY) of photosynthetic electron flows through PSI and PSII were separately assessed in thylakoid membranes isolated from leaves of Cucumis sativus L. (cucumber) that had been chilled in various ways. The QY(PSI) in the thylakoids prepared from the leaves treated at 4° C in moderate light at 220 μmol quanta·m−2·s−1 (400–700 nm) for 5 h, was about 20–30% of that in the thylakoids prepared from untreated leaves, while QY(PSII) decreased, at most, by 20% in response to the same treatment. The decrease in QY(PSI) was observed only when the leaves were chilled at temperatures below 10° C, while such a marked temperature dependency was not observed for the decrease in QY(PSII). In the chilling treatment at 4° C for 5 h, the quantum flux density that was required to induce 50% loss of QY (PSI) was ca. 50 umol quanta·m−2·s−1. When the chilling treatment at 4° C in the light was conducted in an atmosphere of N2, photoinhibition of PSI was largely suppressed, while the damage to PSII was somewhat enhanced. The ferricyanide-oxidised minus ascorbate-reduced difference spectra and the light-induced absorbance changes at 700 nm obtained with the thylakoid suspension, indicated the loss of P700 to extents that corresponded to the decreases in QY(PSI). Accordingly, the decreases in QY(PSI) can largely be attributed to destruction of the PSI reaction centre itself. These results clearly show that, at least in cucumber, a typical chillingsensitive plant, PSI is much more susceptible to aerobic photoinhibition than PSII.

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





primary electron donor of PSI


photosynthetically active photon flux density


quantum yield


  1. Asada, K. (1992) Production and scavenging of active oxygen in chloroplasts. In: Molecular biology of free radical scavenging systems, pp. 173–192, Cold Spring Harbor Laboratory Press, New York

  2. Asada, K., Takahashi, M. (1987) Production and scavenging of active oxygen in photosynthesis. In: Photoinhibition, pp. 227–287, Kyle, D.J., Osmond, C.B., Arntzen, C.J. eds. Elsevier, Amsterdam

  3. Chow, W.S. (1994) Photoprotection and photoinhibitory damage. In: Molecular processes of photosynthesis. Barber, J. ed, JAI Press, Greenwich, Connecticut, in press

  4. Garber, M.P. (1977) Effect of light and chilling temperatures on chilling-sensitive and chilling-resistant plants. Plant Physiol. 59, 981–985

  5. Gerber, D.W., Burris, J.E. (1981) Photoinhibition and P700 in the marine diatom Amphora sp. Plant Physiol. 68, 699–702

  6. Giovanelli, J., San Pietro, A. (1959) Photosynthetic pyridine nucleotide reductase II. Photoinactivation in the presence of chloroplasts. Arch. Biochem. Biophys. 843, 471–485

  7. Hetherington, S.E., He, J., Smillie, R.M. (1989) Photoinhibition at low temperature in chilling-sensitive and -resistant plants. Plant Physiol. 90, 1609–1615

  8. 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

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

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

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

  12. Kaniuga, Z., Sochanowicz, B., Zabek, J., Krzystyniak, K. (1978 a) Photosynthetic apparatus in chilling-sensitive plants. I. Reactivation of Hill reaction activity inhibited on the cold and dark storage of detached leaves and intact plants. Planta 140, 121–128

  13. Kaniuga, Z., Zabek, J., Sochanowicz, B. (1978 b) Photosynthetic apparatus in chilling-sensitive plants. III. Contribution of loosely bound manganese to the mechanism of reversible inactivation of Hill reaction activity following cold and dark storage and illumination of leaves. Planta 144, 49–56

  14. Kislyuk, I.M., Vas'kovskii, M.D. (1972) Effect of cooling cucumber leaves on photosynthesis and photochemical reaction. Soviet Plant Physiol. 191, 688–692 (Fiziol. Rast. 19, 813–818)

  15. Krause, G.H., Köster, S., Wong, S.C. (1985) Photoinhibition of photosynthesis under anaerobic conditions studied with leaves and chloroplasts of Spinada oleracea L. Planta 165, 430–438

  16. Margulies, M.M. (1972) Effect of cold-storage of bean leaves on photosynthetic reactions of isolated chloroplasts. Inability to donate electrons to photosystem II and relation to manganese content. Biochim. Biophys. Acta 267, 96–103

  17. Margulies, M.M., Jagendorf, A.T. (1960) Effect of bean leaves on photosynthetic reaction of isolated chloroplasts. Arch. Biochem. Biophys. 90, 176–183

  18. Ooms, J.J.J., Vredenberg, W.J., Buurneijer, W.F. (1989) Evidence for an electrogenic and a non-electrogenic component in the slow phase of the P515 response in chloroplasts. Photosynth. Res. 20, 119–128

  19. Öquist, G., Greer, D.H., Ögren, E. (1987) Light stress at low temperature. In: Photoinhibition, pp. 67–87, Kyle, D.J., Osmond, C.B., Arntzen, C.J. eds. Elsevier, Amsterdam

  20. Porra, R.J., Thompson, W.A., Kriedemann, P.E. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975, 384–394

  21. Peeler, T.C., Naylor, A.W. (1988) 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

  22. Petering, D., Fee, J.A., Palmer, G. (1971) The oxygen sensitivity of spinach ferredoxin and other iron-sulfur proteins. The formation of protein-bound sulfur-zero. J. Biol. Chem. 246, 643–653

  23. Sakihama, N., Ohmori, H., Sugimoto, N., Yamasaki, Y., Ohsino, R., Shin, M. (1983) Toyopearl HW-65: ammonium sulfate as a new column Chromatographic adsorbent for enzyme purifications. J. Biochem. 93, 129–134

  24. Scheibe, R. (1990) Light/dark modulation: Regulation of chloroplast metabolism in a new light. Bot. Acta 103, 327–334

  25. Sassenrath, G.F., Ort, D.R., Portis, A.R. Jr. (1990) Impaired reductive activation of stromal bisphosphatases in tomato leaves following low-temperature exposure at high light. Arch. Biochem. Biophys. 282, 302–308

  26. Satoh, Ka., Fork, D.C. (1982) Photoinhibition of reaction centers of photosystems I and II in intact Bryopsis chloroplasts under anaerobic conditions. Plant Physiol. 70, 1004–1008

  27. Satoh, Ki. (1970 a) Mechanism of photoinactivation in photosynthetic systems. I. The dark reaction in photoinactivation. Plant Cell Physiol. 11, 15–27

  28. Satoh, Ki. (1970 b) Mechanism of photoinactivation in photosynthetic systems. II. The occurrence and properties of two different types of photoinactivation. Plant Cell Physiol. 11, 29–38

  29. Satoh, Ki. (1970 c) Mechanism of photoinactivation in photosynthetic systems. III. Site and mode of photoinactivation in photosystem I. Plant Cell Physiol. 11, 187–197

  30. Satoh, Ki. (1971) Mechanism of photoinactivation in photosynthetic systems. IV. Light-induced changes in the fluorescence transients. Plant Cell Physiol. 12, 13–27

  31. Shen, J.-R., Terashima, I., Katoh, S. (1990) The cause for dark, chilling-induced inactivation of photosynthetic oxygen-evolving system in cucumber leaves. Plant Physiol. 93, 1354–1357

  32. Smillie, R.M., Nott, R. (1979) Assay of chilling injury in wild and domestic tomatoes based on photosystem activity of the chilled leaves. Plant Physiol. 63, 796–801

  33. Sonoike, K., Katoh, S. (1988) Effects of sodium dodecyl sulfate and methyl viologen on the differential extinction coefficient of P-700 — a band shift of chlorophyll a associated with oxidation of P-700. Biochim. Biophys. Acta 935, 61–71

  34. Takahashi, M., Shimura, S., Hamaguchi, Y., Fujita, Y. (1971) Photoinhibition of phytoplankton photosynthesis as a function of exposure time. J. Oceanogr. Soc. Jpn. 27, 43–50

  35. Terashima, I., Huang, L.-K., Osmond, C.B. (1989 a) Effects of leaf chilling on thylakoid functions, measured at room temperature, in Cucumis sativus L. and Oryza sauva L. Plant Cell Physiol. 30, 841–850

  36. Terashima, I., Shen, J.-R., Katoh, S. (1989 b) Chilling damage in cucumber (Cucumis sativus L.) thylakoids. In: Plant water relations and growth under stress, pp. 470–472, Tazawa, M., Katsumi, M., Masuda, Y., Okamoto, H., eds. Yamada Science Foundation, Osaka and Myu K.K., Tokyo

  37. Terashima, I., Kashino, Y., Katoh, S. (1991 a) Exposure of leaves of Cucumis sativus L. to low temperatures in the light causes uncoupling of thylakoids. I. Studies with isolated thylakoids. Plant Cell Physiol. 32, 1267–1274

  38. Terashima, I., Sonoike, K., Kawazu, T., Katoh, S. (1991 b) Exposure of leaves of Cucumis sativus L. to low temperature in the light causes uncoupling of thylakoids II. Non-destructive measurements in intact leaves. Plant Cell Physiol. 32, 1275–1283

  39. van Hasselt, P.R., van Berlo, H.A.C. (1980) Photooxidative damage to the photosynthetic apparatus during chilling. Physiol. Plant. 50, 52–56

  40. Wise, R.R., Naylor, A.W. (1987 a) Chilling-enhanced photooxidation. The peroxidative destruction of lipids during chilling injury to photosynthesis and ultrastructure. Plant Physiol. 87, 272–277

  41. Wise, R.R., Naylor, A.W. (1987 b) 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

  42. Wise, R.R., Ort, D.R. (1989) Photophosphorylation after chilling in the light. Plant Physiol. 90, 657–664

Download references

Author information

Correspondence to Kintake Sonoike.

Additional information

We are grateful to invaluable comments by Prof. S. Katoh, K. Hikosaka and the members of our laboratory. We also thank A. Aoyama for technical assistance. This work was partly supported by the grants from the Ministry of Education, Science, and Culture, Japan, to I. Terashima (#03740342 and #04640621).

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Terashima, I., Funayama, S. & Sonoike, K. The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II. Planta 193, 300–306 (1994).

Download citation

Key words

  • Chilling stress
  • Cucumis (Cucurbitaceae, cucumber)
  • Photosynthesis
  • Thylakoid
  • Photoinhibition
  • Photosystem I