Skip to main content
Log in

The effects of photoinhibition on the photosynthetic light-response curve of green plant cells (Chlamydomonas reinhardtii)

  • Published:
Planta Aims and scope Submit manuscript

Abstract

The photosynthetic response to light can be accurately defined in terms of (1) the initial slope (quantum yield); (2) the asymptote (light-saturated rate); (3) the convexity (rate of bending); and (4) the intercept (dark respiration). The effects of photoinhibition [which damages the reaction centre of photosystem II (PSII)] on these four parameters were measured in optically thin cultures of green plant cells (Chlamydomonas reinhardtii). The convexity of the light-response curve decreased steadily from a value of 0.98 (indicating a sharply bending response) to zero (indicating Michaelis-Menten kinetics) in response to increasing photoinhibition. Photoinhibition was quantified from the quantum yield of inhibited cells relative to that of control cells. The quantum yield was estimated by applying linear regression to low-light data or by fitting a non-rectangular hyperbola. Assuming the initial slope is linear allowed comparison with earlier work. However, as the convexity was lowered this assumption resulted in a significant underestimate of the true quantum yield. Thus, the apparent level of photoinhibition required for a zero convexity and the initial decrease in light-saturated photosynthesis depended upon how the quantum yield was estimated. If the initial slope of the light response was assumed to be linear the critical level of inhibition was 60%. If the linear assumption was not made, the critical level was 40%. At the level of inhibition where the convexity reached zero, the light-saturated rate of photosynthesis also began to decrease, indicating that this level of inhibition caused photosynthesis to be limited at all light intensities by the rate of PSII electron transport. At this level of inhibition the Fm-Fi signal (where Fm is maximal chlorophyll fluorescence and Fi is intermediate chlorophyll fluorescence of dark adapted cells; Briantais et al. 1988) from the fluorescence induction curve was zero and the Fi-Fo signal (where Fo is initial chlorophyll fluorescence of dark adapted cells) was 30% of the control, indicating dramatic reduction or complete elimination of one type of PSII. These data do not contradict published mathematical models showing that the ratio of the maximum speed of electron transport in PSII relative to the maximum speed of plastoquinone electron transport can determine the convexity of the photosynthetic response to light.

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.

Similar content being viewed by others

Abbreviations

Chl:

chlorophyll content

DCMU:

3-(3,4-dichlorophenyl)-1,1-dimethylurea

Fo, Fi, Fm :

initial, intermediate, and maximal Chl fluorescence of dark adapted cells

P:

rate of net photosynthesis per unit chlorophyll (μmol-(mg Chl)−1 · s−1)

PSII:

photosystem II

PQ:

plastoquinone

Φ :

initial slope to the light-response curve

θ :

convexity (rate of bending) of the light-response curve of photosynthesis

Q:

photosynthetically active photon flux density (400–700 nm, μmol · m−2 · −1)

References

  • Albertsson, P.-Å., Yu, S.-G. (1988) Heterogeneity among Photosystem IIα. Isolation of thylakoid membrane vesicles with different functional antennae size of Photosystem IIα. Biochim. Biophys. Acta 936, 215–221

    Google Scholar 

  • Arnon, D.I. (1949) Copper enzymes in isolated chloroplasts. Polyphenol-oxidase in Beta vulgaris Plant Physiol. 24, 1–15

    Google Scholar 

  • Björkman, O., Demmig, B. (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170, 489–504

    Google Scholar 

  • Björkman, O., Demmig, B., Andrews, T.J. (1988) Mangrove photosynthesis: response to high-irradiance stress. Aust. J. Plant. Physiol. 15, 43–61

    Google Scholar 

  • Black, M.T., Brearley, T.H., Horton, P. (1986) Heterogeneity in chloroplast photosystem II. Photosynth. Res 8, 193–207

    Google Scholar 

  • Briantais, J.-M., Comic, G., Hodges, M. (1988) The modification of chlorophyll fluorescence of Chlamydomonas reinhardtii by photoinhibition and chloramphenicol addition suggests a form of photosystem II less susceptible to degradation. FEBS Lett. 236, 226–230

    Google Scholar 

  • Draper, N.R., Smith, H. (1966) Applied regression analysis. Wiley, New York

    Google Scholar 

  • Erickson, J.M., Pfister, K., Rahire, M., Togasaki, R.K., Mets, L., Rochaix, J.-D. (1989) Molecular and biophysical analysis of herbicide-resistant mutants of Chlamydomonas reinhardtii: Structure-function relationship of the photosystem II D1 polypeptide. Plant Cell 1, 361–371

    Google Scholar 

  • Evans, J.R., Sharkey, T.D., Berry, J.A., Farquhar, G.D. (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Aust. J. Plant Physiol. 13, 281–292

    Google Scholar 

  • Falk, S., Samuelsson, G., Öquist, G. (1990) Temperature-dependent photoinhibition and recovery of photosynthesis in green alga: Chlamydomonas reinhardtii acclimated to 12 and 27° C. Physiol. Plant. 78, 173–180

    Google Scholar 

  • Farquhar, G.D., Wong, S.C. (1984) An empirical model of stomatal conductance. Aust. J. Plant Physiol. 11, 191–210

    Google Scholar 

  • Forti, G. (1987) Energy conversion in higher plants and algae. In: Photosynthesis, pp. 1–20, Amesz, J., ed. Elsevier, Amsterdam New York

    Google Scholar 

  • Heber, U., Neimanis, S., Dietz, K.-J. (1988) Fractional control of photosynthesis by the Qb protein, the cytochrome f/b6 complex and other components of the photosynthetic apparatus. Planta 173, 267–274

    Google Scholar 

  • Herron, H.A., Mauzerall, D. (1972) The development of photosynthesis in a greening mutant of Chlorella and an analysis of the light saturation curve. Plant Physiol. 50, 141–148

    Google Scholar 

  • Johnson, I.R., Parsons, A.J., Ludlow, M.M. (1989) Modelling photosynthesis in monocultures and mixtures. Aust. J. Plant Physiol. 16, 501–516

    Google Scholar 

  • Kaska, D.D., Gunzler, V., Kivirikko, K.I., Myllylä, R. (1987) Characterization of a low-relative-molecular-mass prolyl 4-hydroxylase from the green alga Chlamydomonas reinhardtii. Biochem. J. 241, 483–490

    Google Scholar 

  • Kok, B. (1956) On the inhibition of photosynthesis by intense light. Biochim. Biophys. Acta 21, 234–244

    Google Scholar 

  • Krause, G.H. (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol. Plant. 74, 566–574

    Google Scholar 

  • Laisk, A., Niilisk, H. (1981) Modeling of the stationary and transient kinetics of C3-photosynthesis. In: Photosynthesis IV. Regulation of carbon metabolism, pp. 177–186, Akoyunoglou, G., ed. Balaban International Science Services, Philadelphia

    Google Scholar 

  • Leverenz, J.W. (1987) Chlorophyll content and the light response curve of shade-adapted conifer needles. Physiol. Plant. 71, 20–29

    Google Scholar 

  • Leverenz, J.W. (1988) The effects of illumination sequence, CO2 concentration, temperature and acclimation on the convexity of the photosynthetic light response curve. Physiol Plant. 74, 332–341

    Google Scholar 

  • Leverenz, J.W., Jarvis, P.G. (1979) Photosynthesis in Sitka spruce VIII. The effects of light flux density and direction on the rate of net photosynthesis and the stomatal conductance of needles. J. Appl. Ecol. 16, 919–932

    Google Scholar 

  • Lidholm, J., Gustafsson, P., Öquist, G. (1987) Photoinhibition of photosynthesis and its recovery in the green algae Chlamydomonas reinhardtii. Plant Cell Physiol. 28, 1133–1140

    Google Scholar 

  • Ludlow, M.M., Wilson, G.L. (1971) Photosynthesis of tropical pasture plants. II. Temperature and illumination history. Aust. J. Biol. Sci. 24, 1065–1075

    Google Scholar 

  • Mäenpää, P., Andersson, B., Sundby, C. (1987) Difference in sensitivity to photoinhibition between photosystem II in the apressed and non-appressed thylakoid regions. FEBS Lett. 215, 31–36

    Google Scholar 

  • Marshall, B., Biscoe, P.V. (1980) A model for C3 leaves describing the dependence of net photosynthesis on irradiance. J. Exp. Bot. 120, 29–39

    Google Scholar 

  • Mathis, P., Rutherford, A.W. (1987) The primary reactions of photosystems I and II of algae and higher plants. In: Photosynthesis, pp. 63–96, Amesz, J., ed. Elsevier, Amsterdam

    Google Scholar 

  • Melis, A. (1985) Functional properties of photosystem IIβ in spinach chloroplasts. Biochim. Biophys. Acta 808, 334–342

    Google Scholar 

  • Neale, P.J., Melis, A. (1986) Algal photosynthetic membrane complexes and the photosynthesis-irradiance curve: A comparison of light-adaptation responses in Chlamydomonas reinhardtii (Chlorophyta). J. Phycol. 22, 531–538

    Google Scholar 

  • Ögren, E., Öquist, G., Hällgren, J.-E. (1984) Photoinhibition of photosynthesis in Lemna gibba as induced by the interaction between light and temperature. I. Photosynthesis in vivo. Physiol. Plant. 62, 181–186

    Google Scholar 

  • Öquist, G., Malmberg, G. (1989) Light and temperature dependent inhibition of photosynthesis in frost-hardened and un-hardened seedlings of pine. Photosynth. Res. 20, 261–277

    Google Scholar 

  • Ort, D.R., Baker, N.R. (1988) Consideration of photosynthetic efficiency at low light as a major determinant of crop photosynthetic performance. Plant Physiol. Biochem. 26, 555–565

    Google Scholar 

  • Oya, V.M., Laisk, A.K. (1976) Adaptation of the photosynthesis apparatus to the light profile in the leaf. Soviet Plant Physiol. 23, 381–386

    Google Scholar 

  • Prioul, J.L., Chartier, P. (1977) Partitioning of transfer and carboxylation components of intracellular resistance to photosynthetic CO2 fixation: A critical analysis of the methods used. Ann. Bot. 41, 789–800

    Google Scholar 

  • Raven, J.A., Samuelsson, G. (1986) Repair of photoinhibitory damage in Anacyctis nidulans 625 (Synechococcus 6301): Relation to catalytic capacity for, and energy supply to, protein synthesis, and implications for μmax and the efficiency of lightlimited growth. New Physiol. 103, 625–643

    Google Scholar 

  • Robichaux, R.H., Pearcy, R.W. (1980) Photosynthetic responses of C3 and C4 species from cool shaded habitats in Hawaii. Oecologia 47, 106–109

    Google Scholar 

  • Samuelsson, G., Lönneborg, A., Gustafsson, P., Öquist, G. (1987) The susceptibility of photosynthesis to photoinhibition and the capacity of recovery in high and low light grown Cyanobacteria, Anasystis nidulans. Plant Physiol. 83, 438–441

    Google Scholar 

  • Sharkey, T. (1985) Photosynthesis in intact leaves of C3 plants: Physics, physiology and rate limitations. Bot. Rev. 51, 53–105

    Google Scholar 

  • Sharp, R.E., Matthews, M.A., Boyer, J.S. (1984) Kok effect and the quantum yield of photosynthesis. Light partially inhibits dark respiration. Plant Physiol. 75, 95–101

    Google Scholar 

  • Terashima, I., Saeki, T. (1985) A new model for leaf photosynthesis incorporating the gradients of light environment and of photosynthetic properties of chloroplasts within a leaf. Ann Bot. 56, 489–499

    Google Scholar 

  • Zhang, J.-X. (1988) Modelling irradiance response of leaf photosynthetic rate in wheat and bamboo. Photosynthetica 22, 526–534

    Google Scholar 

  • Zvalinskii, V.I., Litvin, F.F. (1984) Photosynthetic light curves for different organization to photosynthetic units. Soviet Plant Physiol. 30, 656–665

    Google Scholar 

  • Zvalinskii, V.I., Litvin, F.F. (1988) Dependence of photosynthesis on carbon dioxide concentration, light intensity, and the spectral composition of light. Soviet Plant Physiol. 35, 345–356

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

The present investigation was supported by the Swedish Council for Forestry and Agricultural Research, the Swedish Environmental Protection Board, and the Swedish Natural Science Research Council. We thank Dr. Deborah D. Kaska (Department of Biological Sciences, University of California, Santa Barbara, Calif., USA) for giving us Chlamydomonas algae. We thank Professor G. Öquist (Department of Plant Physiology, University of Umea, Umea, Sweden) for his encouragement, valuable comments and discussion.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Leverenz, J.W., Falk, S., Pilström, CM. et al. The effects of photoinhibition on the photosynthetic light-response curve of green plant cells (Chlamydomonas reinhardtii). Planta 182, 161–168 (1990). https://doi.org/10.1007/BF00197105

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00197105

Key words

Navigation