Skip to main content
Log in

Adjustment of thylakoid plastoquinone content and Photosystem I electron donor pool size in response to growth temperature and growth irradiance in winter rye (Secale cereale L.)

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Winter rye (Secale cereale L. cv Musketeer) grown at 5 °C/250 µmol photons m−2 s−1 exhibited a relative reduction state of PS II comparable to that of rye grown at 20 °C but high light (800 µmol photons m−2 s−1) (1-qP = 0.32) whereas winter rye grown at 20 °C/250 µmol photons m−2 s−1 exhibited values of 1-qP (≈ 0.15) comparable to plants grown at 5 °C but low light (50 µmol photons m−2 s−1). The apparent size of the electron donor pool to PS I, estimated either in vivo or in vitro in the presence of methylviologen by ΔA820 was positively correlated with the relative reduction state of PS II under the steady-state growth conditions. Immunoblotting of rye thylakoid polypeptides indicated that the relative contents of Lhcb1, Lhcb2, D1, Cyt f, PC, PsaA/PsaB heterodimer and the β-subunit of ATPase complex exhibited minimal changes on a Chl basis. In contrast, a 2-fold increase in plastoquinone A content was associated with increasing growth irradiance at growth temperatures of either 5 or 20 °C. We suggest that the increases in the apparent size of the electron donor pool to PS I associated with rye grown at either 5 °C/250 µmol photons m−2 s−1or 20 °C/800 µmol photons m−2 s−1 may be explained by an increased thylakoid plastoquinone A content, coupled with possible enhanced PS I cyclic electron transport and/or increased capacity for electron donation from the stroma to the intersystem electron transport chain. The results are discussed with respect to photosynthetic adjustment to changes in PS II ‘excitation pressure’ in winter rye.

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

References

  • Adams III WW, Hoehn A and Demmig-Adams B (1995) Chilling temperatures and the xanthophyll cycle. A comparison of warm-grown and overwintering spinach. Aust J Plant Physiol 22: 75–85

    Google Scholar 

  • Allen JF, Alxciev K and Håkansson G (1995) Regulation by redox signalling. Curr Biol 5: 869–872

    Google Scholar 

  • Anderson JM (1986) Photoregulation of the composition, function, and structure of thylakoid membranes. Annu Rev Plant Physiol 37: 93–136

    Google Scholar 

  • Anderson JM, Chow WS and Park Y-I (1995) The grand design of photosynthesis: Acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46: 129–139

    Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24: 1–15

    Google Scholar 

  • Asada K, Heber U and Schreiber U (1992) Pool size of electrons that can be donated to P700+, as determined in intact leaves: Donation to P700+ from stromal components via the intersystem chain. Plant Cell Physiol 33: 927–932

    Google Scholar 

  • Burkey KO (1993) Effect of growth irradiance on plastocyanin levels in barley. Photosynth Res 36: 103–110

    Google Scholar 

  • Burkey KO and Wells R (1996) Effects of natural shade on soybean thylakoid membrane composition. Photosynth Res 50: 149–158

    Google Scholar 

  • Campbell D, Zhou G, Gustafsson P, Öquist G and Clarke AK (1995) Electron transport regulates exchange of two forms of Photosystem II D1 protein in the cyanobacterium Synechococcus. EMBO J 14: 5457–5466

    Google Scholar 

  • Chow WS, Melis A and Anderson JM (1990b) Adjustments of photosystem stoichiometry in chloroplasts improve the quantum efficiency of photosynthesis. Proc Natl Acad Sci USA 87: 7502–7506

    Google Scholar 

  • De la Torre WR and Burkey KO (1990) Acclimation of barley to changes in light intensity: Photosynthetic electron transport activity and components. Photosynth Res 24: 127–136

    Google Scholar 

  • Dau H (1994) Short-term adaptation of plants to changing light intensities and its relation to Photosystem II photochemistry and fluorescence emission. J Photochem Photobiol B: Biol 26: 3–27

    Google Scholar 

  • Durford DG and Falkowski PG (1997) Chloroplast redox regulation of nuclear gene transcription during photoacclimation. Photosynth Res 53: 229–241

    Google Scholar 

  • Escoubas J-M, Lomas M, LaRoche J and Falkowski PG (1995) Light intensity regulation of cabgene transcription is signalled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA 92: 10237–10241

    Google Scholar 

  • Fujita Y, Murakami A, Aizawa K and Ohki K (1994) Short-term and long-term adaptation of the photosynthetic apparatus: homeostatic properties of thylakoids. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria, pp 677–692. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Fujita Y, Murakami A and Ohki K (1987) Regulation of photosystem composition in the cyanobacterial photosynthetic system: the regulation occurs in response to the redox state of the electron pool located between the two photosystems. Plant Cell Physiol 28: 283–292

    Google Scholar 

  • Giacometti GM, Barbato R, Chiavamonte S, Friso G and Rigoni F (1996) Effects of ultraviolet-B radiation on Photosystem II of the cyanobacterium Synechocystis sp. PCC 6083. Eur J Biochem 242: 799–806

    Google Scholar 

  • Gray GR, Chauvin LP, Sarhan F and Huner NPA (1997) Cold acclimation and freezing tolerance: A complex interaction of light and temperature. Plant Physiol 114: 467–474

    Google Scholar 

  • Gray GR, Savitch LV, Ivanov AG and Huner NPA (1996) Photosystem II excitation pressure and development of resistance to photoinhibition. II. Adjustment of photosynthetic capacity in winter wheat and winter rye. Plant Physiol 110: 61–71

    Google Scholar 

  • Griffith M, Elfman B and Camm EL (1984) Accumulation of plastoquinone A during low temperature growth of winter rye. Plant Physiol 74: 727–729

    Google Scholar 

  • Guy CL, Huber JLA, Huber SC (1992) Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiol 100: 502–508

    Google Scholar 

  • Huner NPA, Maxwell DP, Gray GR, Savitch LV, Krol M, Ivanov AG and Falk S (1996) Sensing environmental temperature change through imbalances between energy supply and energy consumption: redox state of Photosystem II. Physiol Plant 97: 358–364

    Google Scholar 

  • Huner NPA, Öquist G, Hurry VM, Krol M, Falk S and Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37: 19–39

    Google Scholar 

  • Hurry VM, Strand Å, Tobiæson M, Gardeström P and Öquist G (1995) Cold hardening of spring and winter wheat and rape results in differential effects on growth, carbon metabolism and carbohydrate content. Plant Physiol 109: 697–706

    Google Scholar 

  • Klughammer C and Schreiber U (1994) An improved method, using saturating light pulses, for the determination of Photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192: 261–268

    Google Scholar 

  • Kramer DM and Crofts AR (1996) Control and measurement of photosynthetic electron transport in vivo. In: Baker NR (ed) Advances in Photosynthesis: Photosynthesis and the Environment, Vol 5, pp 25–66. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Krause GH (1994) Photoinhibition induced by low temperatures. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field, pp 331–348. Bios Scientific Publishers, Oxford

    Google Scholar 

  • Krol M and Huner NPA (1985) Growth and development at cold-hardening temperatures. Pigment and benzoquinone accumulation in winter rye. Can J Bot 63: 716–721

    Google Scholar 

  • Krol M, Maxwell DP and Huner NPA (1997) Exposure of Dunaliella salina to low temperature mimics the high lightinduced accumulation of carotenoids and the carotenoid binding protein (Cbr). Plant Cell Physiol 38: 213–216

    Google Scholar 

  • Król M, Spangfort MD, Huner NPA, Öquist G, Gustafsson P and Jansson S (1995) Chlorophyll a/b-binding proteins, pigment conversions, and early light-induced proteins in a chlorophyll b-less barley mutant. Plant Physiol 107: 873–883

    Google Scholar 

  • Lee W-J and Whitmarsh J (1989) Photosynthetic apparatus of pea thylakoid membranes. Response to growth light intensity. Plant Physiol 89: 932–940

    Google Scholar 

  • Machalek KM, Davison IR and Falkowski PG (1996) Thermal acclimation and photoacclimation of photosynthesis in the brown alga Laminaria saccharina. Plant Cell Environ 19: 1005–1016

    Google Scholar 

  • Maxwell DP, Falk S and Huner NPA (1995a) Photosystem II excitation pressure and development of resistance to photoinhibition I. Light-harvesting complex II abundance and zeaxanthin content in Chlorella vulgaris. Plant Physiol 107: 687–694

    Google Scholar 

  • Maxwell DP, Laudenbach DE and Huner NPA (1995b) Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiol 109: 787–795

    Google Scholar 

  • Melis A, Manodori A, Glick RE, Ghirardi ML, McCauley SW and Neale PJ (1985) The mechanism of photosynthetic membrane adaptation to environmental stress conditions: A hypothesis on the role of electron-transport capacity and of ATP/NADPH pool in the regulation of thylakoid membrane organization and function. Physiol Vég 23: 757–765

    Google Scholar 

  • Murakami A, Fujita Y, Nemson JA and Melis A (1997) Chromatic regulation in Chlamydomonas reinhardtii: Time course of photosystem stoichiometry adjustment following a shift in growth light quality. Plant Cell Physiol 38: 188–193

    Google Scholar 

  • Öquist G and Huner NPA (1993) Cold-hardening induced resistance to photoinhibition in winter rye is dependent upon an increased capacity for photosynthesis. Planta 189: 150–156

    Google Scholar 

  • Öquist G, Anderson JM, McCaffery S and ChowWS (1992a) Mechanistic differences in photoinhibition of sun and shade plants. Planta 188: 422–431

    Google Scholar 

  • Öquist G, Chow WS and Anderson JM (1992b) Photoinhibition of photosynthesis represents a mechanism for long-term regulation of Photosystem II. Planta 186: 450–460

    Google Scholar 

  • Öquist G, Greer DH and Ögren E (1987) Light stress at low temperature. In: Kyle DJ, Osmond CB and Arntzen CJ (eds) Photoinhibition, Topics in Photosynthesis, Vol 9, pp 67–88. Elsevier Science Publishers BV (Biomedical Division), Amsterdam

    Google Scholar 

  • Osmond CB (1994) What is photoinhibition? Some insights from comparison of shade and sun plants. In: Baker NR and Bowyer JR (eds) Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field, pp 1–24. Bios Scientific Publishers, Oxford

    Google Scholar 

  • Savitch LV, Maxwell DP and Huner NPA (1996) Photosystem II excitation pressure and photosynthetic carbon metabolism in Chlorella vulgaris. Plant Physiol 111: 127–136

    Google Scholar 

  • Schreiber U, Bilger W and Neubauer C (1994) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Shulze E-D and Caldwell MM (eds) Ecophysiology of Photosynthesis, pp 49–70. Springer-Verlag, Berlin

    Google Scholar 

  • Schreiber U, Klughammer C and Neubauer C (1988) Measuring P700 absorbance changes around 830 nm with a new type of pulse modulation system. Z Naturforsch 43c: 686–698

    Google Scholar 

  • Staub JM and Deng X-W (1996) Light signal transduction in plants. Photochem Photobiol 64: 897–905

    Google Scholar 

  • Walters RG and Horton P (1994) Acclimation of Arabidopsis thaliana to the light environment: Changes in composition of the photosynthetic apparatus. Planta 195: 248–256

    Google Scholar 

  • Walters RG and Horton P (1995) Acclimation of Arabidopsis thaliana to the light environment: Regulation of chloroplast composition. Planta 197: 475–481

    Google Scholar 

  • Wild A, Höpfner M, Rühle W and Richter M (1986) Changes in the stoichiometry of Photosystem II components as an adaptive response to high-light and low-light conditions during growth. Z Naturforsch 41c: 597–603

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gray, G.R., Ivanov, A.G., Król, M. et al. Adjustment of thylakoid plastoquinone content and Photosystem I electron donor pool size in response to growth temperature and growth irradiance in winter rye (Secale cereale L.). Photosynthesis Research 56, 209–221 (1998). https://doi.org/10.1023/A:1006049925042

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006049925042

Navigation