Skip to main content
SpringerLink
Log in

Photosynthetic response of Chlamydomonas reinhardtii to short-term storage on ice in darkness. Dependence of the response on growth conditions

  • Research Papers
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

The effect of storage of the unicellular green alga Chlamydomonas reinhardtii (strain 137+) in the pelleted state in darkness on ice (0.2–0.5°C) (further simply “SPDI-treatment”) on its photosynthetic and respiratory activities was studied. To this end, the steady-state rates of O2 exchange in darkness (dark respiration) and under saturating light (apparent photosynthesis) as well as the induction periods (IP) of apparent photosynthesis were measured at 25°C in the SPDI-untreated and SPDI-treated for the period from ∼0.5 to ∼30 h algal cells. In contrast to expectations, the SPDI-treatment consistently affected the rate and IP of photosynthesis depending on the physiological state of C. reinhardtii. Dark respiration was affected by the SPDI-treatment as well. However, in absolute values the respiratory changes were much less than the photosynthetic ones, and they were insufficiently reproducible. The SPDI-treatment affected photosynthesis most significantly in high-CO2-grown cells (cells grown at 5% CO2 in white light). The rate of photosynthesis in these cells declined quasi-exponentially as a function of time during the SPDI-treatment with a t 1/2 ∼1.5 h and finally became by about 60% lower than that before the SPDI-treatment. This decline of photosynthesis was accompanied by continuous and essential increase in the photosynthetic IP. The SPDI-induced photosynthetic changes in high-CO2-grown cells resulted from the firm disfunction of the photosynthetic apparatus. After switch from growth at 5% CO2 in white light to growth at ∼0.03% CO2 (air) in white, blue, or red light, the alga gradually transited to a physiological state, in which the negative effects of the SPDI-treatment on the rate and IP of photosynthesis became weak and absent, respectively. Remarkably, this transition was faster in blue (≤5 h) than in white and red light (>10 h). Similar changes in the response of the alga to the SPDI-treatment occurred when high-CO2-grown cells (5% CO2, white light, 26°C) were incubated in darkness (air, 24–26°C) for 20–25 h. The results of study were analyzed in the light of literature data relating to the effects of CO2 concentration, darkness, and light quality on carbohydrates in plant organisms. The analysis led to suggestion that there is connection between the negative effect of the SPDI-treatment on C. reinhardtii and nonstructural carbohydrates presented in the alga: the more carbohydrates contain the alga, the more extensive inactivation of the photosynthetic apparatus occurs in it during its storage in the dense (pelleted) state in darkness on ice.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

Chl:

chlorophyll

Ci :

dissolved inorganic carbon

IP:

induction period of photosynthesis

PFD:

photon flux density

PSII:

photosystem II

SPDI:

storage of pelleted cells in darkness on ice

References

  1. Borodin, V.B., Effect of Red and Blue Light on Acclimation of Chlamydomonas reinhardtii to CO2-Limiting Conditions, Russ. J. Plant Physiol., 2008, vol. 55, pp. 441–448.

    Article  CAS  Google Scholar 

  2. Borodin, V., Gardeström, P., and Samuelsson, G., The Effect of Light Quality on the Induction of Efficient Photosynthesis under Low CO2 Conditions in Chlamydomonas reinhardtii and Chlorella pyrenoidosa Physiol. Plant., 1994, vol. 92, pp. 254–260.

    Article  CAS  Google Scholar 

  3. Sueoka, N., Mitotic Replication of Deoxyribonucleic Acid in Chlamydomonas reinhardtii, Proc. Natl. Acad. Sci. USA, 1960, vol. 46, pp. 83–91.

    Article  CAS  Google Scholar 

  4. Hutner, S.H., Provasoli, L., Schatz, A., and Haskins, C.P., Some Approaches to the Study of the Role of Metals in the Metabolism of Microorganisms, Proc. Am. Philos. Soc., 1950, vol. 94, pp. 152–170.

    CAS  Google Scholar 

  5. Porra, R.J., Thompson, W.A., and Kriedemann, P.E., 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, 1989, vol. 975, pp. 384–394.

    Article  CAS  Google Scholar 

  6. Borodin, V. and Hurry, V., Regulation of Chilling Sensitivity of Chlamydomonas reinhardtii by CO2 and Light, Int. Meet. Photosynthesis in the Post-Genomic Era: Structure and Function of Photosystems, Pushchino, 2006, p. 236.

    Google Scholar 

  7. Edwards, G. and Walker, D.A., C3, C4: Mechanisms, and Cellular and Environmental Regulation of Photosynthesis, Oxford: Blackwell, 1983.

    Google Scholar 

  8. Kirschbaum, M.U.F., Köppers, M., Schneider, H., Giersch, C., and Noe, S., Modelling Photosynthesis in Fluctuating Light with Inclusion of Stomatal Conductance, Biochemical Activation and Pools of Key Photosynthetic Intermediates, Planta, 1998, vol. 204, pp. 16–26.

    Article  CAS  Google Scholar 

  9. Yamori, W., Masumoto, C., Fukayama, H., and Makino, A., Rubisco Activase Is a Key Regulator of Non-Steady-State Photosynthesis at Any Leaf Temperature and, to a Lesser Extent, of Steady-State Photosynthesis at High Temperature, Plant J., 2012, vol. 71, pp. 871–880.

    Article  PubMed  CAS  Google Scholar 

  10. Makino, A., Miyake, C., and Yokota, A., Physiological Functions of the Water-Water Cycle (Mehler Reaction) and the Cyclic Electron Flow around PSI in Rice Leaves, Plant Cell Physiol., 2002, vol. 43, pp. 1017–1026.

    Article  PubMed  CAS  Google Scholar 

  11. Gardeström, P., Igamberdiev, A.U., and Raghavendra, A.S., Mitochondrial Functions in the Light and Significance to Carbon-Nitrogen Interactions, Advances in Photosynthesis and Respiration, vol. 12, Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism, Foyer, C. and Noctor, G., Eds., Dordrecht: Kluwer, 2002, pp. 151–172.

    Google Scholar 

  12. Forti, G., The Role of Respiration in the Activation of Photosynthesis upon Illumination of Dark Adapted Chlamydomonas reinhardtii, Biochim. Biophys. Acta, 2008, vol. 1777, pp. 1449–1454.

    Article  PubMed  CAS  Google Scholar 

  13. Cardol, P., de Paepe, R., Franck, F., Forti, G., and Finazzi, G., The Onset of NPQ and ΔμH+ upon Illumination of Tobacco Plants Studied through the Influence of Mitochondrial Electron Transport, Biochim. Biophys. Acta, 2010, vol. 1797, pp. 177–188.

    Article  PubMed  CAS  Google Scholar 

  14. Terashima, I., Huang, L.-K., and Osmond, C.B., Effects of Leaf Chilling on Thylakoid Functions, Measured at Room Temperature, in Cucumis sativus L. and Oryza sativa L., Plant Cell Physiol., 1989, vol. 30, pp. 841–850.

    CAS  Google Scholar 

  15. Kowallik, W., Blue Light Effects on Respiration, Annu. Rev. Plant Physiol., 1982, vol. 33, pp. 51–72.

    Article  CAS  Google Scholar 

  16. Chen, M., Chory, J., and Fankhauser, C., Light Signal Transduction in Higher Plants, Annu. Rev. Genet., 2004, vol. 38, pp. 87–117.

    Article  PubMed  CAS  Google Scholar 

  17. Christie, J.M., Phototropin Blue-Light Receptors, Annu. Rev. Plant Biol., 2007, vol. 58, pp. 21–45.

    Article  PubMed  CAS  Google Scholar 

  18. Matsuda, R., Ohashi-Kaneko, K., Fujiwara, K., and Kurata, K., Analysis of the Relationship between Blue-Light Photon Flux Density and the Photosynthetic Properties of Spinach (Spinacia oleracea L.) Leaves with Regard to the Acclimation of Photosynthesis to Growth Irradiance, Soil Sci. Plant Nutr., 2007, vol. 53, pp. 459–465.

    Article  CAS  Google Scholar 

  19. Matsuda, R., Ohashi-Kaneko, K., Fujiwara, K., and Kurata, K., Effects of Blue-Light Photon Flux Density on Nitrogen and Carbohydrate Content and Growth of Spinach, Acta Hortic., 2008, vol. 801, pp. 1393–1398.

    CAS  Google Scholar 

  20. Hogewoning, S.W., Trouwborst, G., Maljaars, H., Poorter, H., van Ieperen, W., and Harbinson, J., Blue Light Dose-Responses of Leaf Photosynthesis, Morphology, and Chemical Composition of Cucumis sativus Grown under Different Combinations of Red and Blue Light, J. Exp. Bot., 2010, vol. 61, pp. 3107–3117.

    Article  PubMed  CAS  Google Scholar 

  21. Kuchitsu, K., Tsuzuki, M., and Miyachi, S., Changes of Starch Localization within the Chloroplast Induced by Changes in CO2 Concentration during Growth of Chlamydomonas reinhardtii: Independent Regulation of Pyrenoid Starch and Stroma Starch, Plant Cell Physiol., 1988, vol. 29, pp. 1269–1278.

    CAS  Google Scholar 

  22. Geraghty, A.M. and Spalding, M.H., Molecular and Structural Changes in Chlamydomonas under Limiting CO2. A Possible Mitochondrial Role in Adaptation, Plant Physiol., 1996, vol. 111, pp. 1339–1347.

    PubMed  CAS  Google Scholar 

  23. Thyssen, C., Schlichting, R., and Giersch, C., The CO2-Concentrating Mechanism in the Physiological Context: Lowering the CO2 Supply Diminishes Culture Growth and Economises Starch Utilization in Chlamydomonas reinhardtii, Planta, 2001, vol. 213, pp. 629–639.

    Article  PubMed  CAS  Google Scholar 

  24. Oyama, Y., Izumo, A., Fujiwara, S., Shimonaga, T., Nakamura, Y., and Tsuzuki, M., Granule-Bound Starch Synthase cDNA in Chlorella kessleri 11 h: Cloning and Regulation of Expression by CO2 Concentration, Planta, 2006, vol. 224, pp. 646–654.

    Article  PubMed  CAS  Google Scholar 

  25. Ricketts, T.R., On the Chemical Composition of Some Unicellular Algae, Phytochemistry, 1966, vol. 5, pp. 67–76.

    Article  CAS  Google Scholar 

  26. Klein, U., Intracellular Carbon Partitioning in Chlamydomonas reinhardtii, Plant Physiol., 1987, vol. 85, pp. 892–897.

    Article  PubMed  CAS  Google Scholar 

  27. Huppe, H.C. and Turpin, D.H., Integration of Carbon and Nitrogen Metabolism in Plant and Algal Cells, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1994, vol. 45, pp. 577–607.

    Article  CAS  Google Scholar 

  28. Wilhelm, C., Kramer, P., and Wild, A., Effect of Different Light Qualities on the Ultrastructure, Thylakoid Membrane Composition and Assimilation Metabolism of Chlorella fusca, Physiol. Plant., 1985, vol. 64, pp. 359–364.

    Article  CAS  Google Scholar 

  29. Hema, R., Senthil-Kumar, M., Shivakumar, S., Chandrasekhara, Reddy, P., and Udayakumar, M., Chlamydomonas reinhardtii, a Model System for Functional Validation of Abiotic Stress Responsive Genes, Planta, 2007, vol. 226, pp. 655–670.

    Article  PubMed  CAS  Google Scholar 

  30. Kreslavski, V.D., Carpentier, R., Klimov, V.V., Murata, N., and Allakhverdiev, S.I., Molecular Mechanisms of Stress Resistance of the Photosynthetic Apparatus, Biochemistry (Moscow), Suppl. ser. A: Membrane and Cell Biol., 2007, vol. 24, pp. 185–205.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Basic Problems of Biology, Russian Academy of Sciences, Institutskaya ul. 2, Pushchino, Moscow oblast, 142290, Russia

    V. B. Borodin

Authors
  1. V. B. Borodin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. B. Borodin.

Additional information

Original Russian Text © V.B. Borodin, 2013, published in Fiziologiya Rastenii, 2013, Vol. 60, No. 3, pp. 434–445.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Borodin, V.B. Photosynthetic response of Chlamydomonas reinhardtii to short-term storage on ice in darkness. Dependence of the response on growth conditions. Russ J Plant Physiol 60, 420–430 (2013). https://doi.org/10.1134/S1021443713030035

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443713030035

Keywords

Search

Navigation