Skip to main content
Log in

Thylakoid membrane energization and swelling in photoinhibited Chlamydomonas cells is prevented in mutants unable to perform cyclic electron flow

  • Regular paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Photoinhibition of Photosystem II in unicellular algae in vivo is accompanied by thylakoid membrane energization and generation of a relatively high ΔpH as demonstrated by 14C-methylamine uptake in intact cells. Presence of ammonium ions in the medium causes extensive swelling of the thylakoid membranes in photoinhibited Chlamydomonas reinhardtii but not in Scenedesmus obliquus wild type and LF-1 mutant cells. The rise in ΔpH and the related thylakoid swelling do not occur at light intensities which do not induce photoinhibition. The rise in ΔpH and membrane energization are not induced by photoinhibitory light in C. reinhardtii mutant cells possessing an active Photosystem II but lacking cytochrome b6/f, plastocyanin or Photosystem I activity and thus being unable to perform cyclic electron flow around Photosystem I. In these mutants the light-induced turnover of the D1 protein of Reaction Center II is considerably reduced. The high light-dependent rise in ΔpH is induced in the LF-1 mutant of Scenedesmus which can not oxidize water but otherwise possesses an active Reaction Center II indicating that PS II-linear electron flow activity and reduction of plastoquinone are not required for this process. Based on these results we conclude that photoinhibition of Photosystem II activates cyclic electron flow around Photosystem I which is responsible for the high membrane energization and ΔpH rise in cells exposed to excessive light intensities.

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

cyt b6/f:

cytochrome b6/f

Diuron:

3-(3,4-dichlorophenyl)-1 dimethyl urea

QB :

the secondary quinone acceptor of reaction center II

DNP:

2,4,Dinitrophenol

FCCP:

carbonyl cyanide trifluoromethoxy phenylhydrazone

SDS-PAGE:

sodium dodecylsulfate polyacrylamide gel electrophoresis

References

  • Asada K, Neubauer C, Heber U and Schreiber U (1990) Methyl viologen-dependent cyclic electron transport in spinach chloroplasts in the absence of oxygen. Plant Cell Physiol 31: 557–564

    Google Scholar 

  • Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci USA 79: 4352–4356

    Google Scholar 

  • Boussiba S and Gibson J (1991) Ammonia translocation in Synechococcus R-2(PC7942). FEMS Microbiol Lett 43: 289–293

    Article  Google Scholar 

  • Callahan FE, Becker DW and Cheniae GFM (1986) Studies on the photoactivation of the water-oxidising enzyme. II. Characterization of weak light photoinhibition of PS II and its light-induced recovery. Plant Physiol 82: 261–269

    Google Scholar 

  • Canaani O and Havaux M (1990) Evidence for a biological role in photosynthesis for cytochrome b 559, a component of Photosystem II reaction center. Proc Natl Acad Sci USA 87: 9295–9299

    PubMed  Google Scholar 

  • Canaani O, Schuster G and Ohad I (1989) Photoinhibition in Chlamydomonas reinhardtii: effect on state transitions, intersystem energy distribution, and Photosystem I cyclic electron flow. Photosynth Res 20: 129–146

    Google Scholar 

  • Demeter S and Govindjee (1989) Thermoluminescence in Plants. Physiol Plant 75: 121–130

    Google Scholar 

  • Diner BA, Ries DF, Cohen BN and Metz JG (1988) COOH-terminal processing of polypeptide D1 of Photosystem II reaction center of Scenedesmus obliquus is necessary for the assembly of the oxygen evolving-complex. J Biol Chem 263: 8972–8980

    PubMed  Google Scholar 

  • Falkowski PG, Fujita Y, Ley A and Mauzeral D (1986) Evidence for cyclic electron flow around Photosystem II in Chlorella pyrenoidosa. Plant Physiol 81: 310–312

    Google Scholar 

  • Florencio FJ and Vega JM (1983) Utilization of nitrate, nitrite and ammonium by Chlamydomonas reinhardtii. Planta 158: 288–293

    Google Scholar 

  • Garab G, Lajko F, Mustardy L and Marton L (1989) Respiratory control over photosynthetic electron transport in chloroplasts of higher-plant cells: evidence for chlororespiration. Planta 179: 349–358

    Google Scholar 

  • Gong H and Ohad I (1992) The PO/POH2 ratio and occupancy of photosystem II-QB site by plastoquinone control the degradation of the D1 protein during photoinhibition in vivo. J Biol Chem 266: 21293–21299

    Google Scholar 

  • Heber U, Egneus H, Hanck U, Jensen M and Koster S (1978) Regulation of photosynthetic electron transport and photophosphorylation in intact chloroplasts and leaves of Spinacia oleracea L. Planta 143: 41–49

    Google Scholar 

  • Herbert SK, Fork DC and Malkin S (1990) Photoacoustic measurements in vivo of energy storage by cyclic electron flow in algae and higher plants. Plant Physiol 94: 926–934

    Google Scholar 

  • Jegerschöld C, Virgin I and Styring S (1990) Light dependent degradation of the D1 protein in Photosystem II is accelerated after inhibition of the water splitting reaction. Biochemistry 29: 6179–6186

    PubMed  Google Scholar 

  • Krause GH and Behrend U (1986) Delta pH dependent chlorophyll fluorescence queching indicating a mechanism of protection against photoinhibition of chloroplasts. FEBS Lett 200: 298–302

    Article  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685

    PubMed  Google Scholar 

  • Levine RP and Goodenough UW (1970) The genetics of photosynthesis and the chloroplast in Chamydomonas reinhardtii. Ann Rev Gen 4: 397–408

    Article  Google Scholar 

  • Maione TE and Gibbs M (1986) Association of the chloroplastic and photosynthetic electron transport chains of Chlamydomonas reinhardtii with photoreduction and the oxyhydrogen reaction. Plant Physiol 80: 364–368

    Google Scholar 

  • McCauley S, Melis A, Tang GM-S and Arnon DI (1987) Protonophores induce plastoquinol oxidation and quench chloroplast fluorescence: Evidence for a cyclic, proton-conducting pathway in oxygenic photosynthesis. Proc Natl Acad Sci USA 84: 8424–8428

    Google Scholar 

  • Myers J (1987) Is there significant cyclic electron flow around photoreaction I in cyanobacteria? Photosynth Res 14: 55–69

    Google Scholar 

  • Nissani E and Ginsburg H (1989) Protonophoric effects of antimalarial drugs and alkylamines in Escherichia coli membranes. Biochim Biophys Acta 978: 293–298

    PubMed  Google Scholar 

  • Noctor G and Horton P (1990) Uncoupler titration of energy-dependent chlorophyll fluorescence quenching and Photosystem II photochemical yield in intact pea chloroplasts. Biochim Biophys Acta 1016: 228–234

    Google Scholar 

  • Ohad I, Siekevitz P and Palade GE (1967) Biogenesis of chloroplast membranes. 1. Plastid dedifferentiation in a dark grown algae mutant (Chlamydomonas reinhardtii). J Cell Biol 35: 553–584

    Article  PubMed  Google Scholar 

  • Ohad I, Adir N, Koike H, Kyle DJ and Inoue Y (1990) Mechanism of Photoinhibition in vivo. J Biol Chem 265: 1972–1979

    PubMed  Google Scholar 

  • Oxborough K and Horton P (1987) Characterization of the effects of antimycin A upon high energy state quenching of chlorophyll fluorescence (qE) in spinach and pea chloroplasts. Photosynth Res 12: 119–127

    Google Scholar 

  • Rottenberg H, Grunwald T and Avron M (1972) Determination of delta pH in chloroplasts 1. Distribution of [14C]Methylamine. Eur J Biochem 25: 54–63

    PubMed  Google Scholar 

  • Rutherford AW, Renger G, Koike H and Inoue Y (1984) Thermoluminescence as a probe of Photosystem II: The redox and protonation states of the secondary acceptor quinone and the O2-evolving enzyme. Biochim Biophys Acta 767: 548–556

    Google Scholar 

  • Schonknecht G, Hedrich R, Junge W and Raschke K (1988) A voltage-dependent chloride channel in the photosynthetic membrane of a higher plant. Nature 336: 589–592

    Article  Google Scholar 

  • Schreiber U, Reising H and Neubauer C (1991) Contrasting pH optima of light-driven O2 and O2H2-reduction in spinach chloroplasts as measured via chlorophyll fluorescence. Z Naturforsch 46: 173–180

    Google Scholar 

  • Schuster G, Timberg R and Ohad I (1988) Turnover of thylakoid Photosystem II proteins during photoinhibition of Chlamydomonas reinhardtii. Eur J Biochem 177: 403–10

    PubMed  Google Scholar 

  • Shochat S, Adir N, Gal A, Inoue Y, Mets L and Ohad I (1990) Photoinactivation of Photosystem II and degradation of the D1 protein are reduced in a cytochrome b6/f-less mutant of Chlamydomonas reinhardtii. Z Naturforsch 45c: 395–401

    Google Scholar 

  • Slovacek RE, Crowther D and Hind G (1980) Relative activities of linear and cyclic electron flows during chloroplast CO2-fixation. Biochim Biophys Acta 592: 495–505

    PubMed  Google Scholar 

  • Spreitzer RJ and Mets L (1981) Photosynthesis-deficient mutants of Chlamydomonas reinhardtii with associated light-sensitive phenotypes. Plant Physiol 67: 565–569

    Google Scholar 

  • Takahama U, Shimizu-Takahama M and Heber U (1981) The redox state of the NADP system in illuminated chloroplasts. Biochim Biophys Acta 637: 530–539

    Google Scholar 

  • Vass I, Mohanty N and Demeter S (1988) Photoinhibition of electron transport activity of Photosystem II in isolated thylakoids studied by thermoluminescence and delayed luminescence. Z Naturforsch 43c: 871–876

    Google Scholar 

  • Weis E and Berry J (1987) Quantum efficiency of Photosystem II in relation to ‘energy-dependent’ quenching of chlorphyll fluorescence. Biochim Biophys Acta 894: 198–208

    Google Scholar 

  • Weis E, Bali JT and Berry J (1987) Photosynthetic control of electron transport in leaves of Phaseolus vulgaris: evidence for regulation of Photosystem II by the proton gradient. In: Biggins J (ed) Progress in Photosynthesis Research, Vol 2, pp 553–556. Martinus Nijhoff, Dordrecht

    Google Scholar 

  • Yin Z-H, Siebke K and Heber U (1991) Light dependent pH changes in leaves of C3 plants. Planta 184: 30–34

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Itzhak Ohad.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Topf, J., Gong, H., Timberg, R. et al. Thylakoid membrane energization and swelling in photoinhibited Chlamydomonas cells is prevented in mutants unable to perform cyclic electron flow. Photosynth Res 32, 59–69 (1992). https://doi.org/10.1007/BF00028798

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00028798

Key words

Navigation