Skip to main content
Log in

Oxygen-evolving system and secondary quinonic acceptors are highly reduced in dark adapted Euglena cells: A thermoluminescence study

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

Abstract

Characteristics of thermoluminescence glow curves were compared in three types of Euglena cells: (i) strictly autotrophic, Cramer and Myers cells; (ii) photoheterotrophic cells sampled from an exponentially growing culture containing lactate as substrate repressing the photosynthetic activity; (iii) semiautotrophic cells, sampled when the lactate being totally exhausted, the photosynthesis was enhanced.

In autotrophic and semiautotrophic cells, composite curves were observed after series of two or more actinic flashes fired at −10°C, which can be deconvoluted into a large band peaking in the range 12–22°C and a smaller one near 40°C, This second band presents the characteristics of a typical B band (due to S2/3QB - recombination), whereas the first one resembled the band, shifted by -15–20°C, which is observed in herbicide resistant plants. The amplitude of this major band, which was in all cases very low after one flash, exhibited oscillations of period four but rapidly damping, with maxima after two and six flashes. In contrast, photoheterotrophic Euglena displayed single, non-oscillating curves with maxima in the range 5–10°C.

In autotrophic and semiautotrophic cells, oxidizing pretreatments by either a preillumination with one or more (up to twenty-five) flashes, or a far-red preillumination in the presence of methylviologen, followed by a short dark period, induced thermoluminescence bands almost single and shifted by +3–5°C, or +12°C, respectively. In autotrophic cells, far-red light plus methyl viologen treatment induced a band peaking at 31°C, as in isolated thylakoids from Euglena or higher plants, while it had barely any effect in photoheterotrophic cells.

Due to metabolic activities in dark-adapted cells, a reduction of redox groups at the donor and acceptor sides of PS II dark-adapted cells is supposed to occur. Two different explanations can be proposed to explain such a shift in the position of the main band in dark-adapted autotrophic control. The first explanation would be that in these reducing conditions a decreasing value of the equilibrium constant for the reaction: SnQA -QB⇌SnQAQB -, would determine the shift of the main TL band towards low temperatures, as observed in herbicide resistant material. The second explanation would be that the main band would correspond to ‘peak III’ already observed in vivo and assigned to S2/3QB 2- recombinations.

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

CM:

Cramer and Myers

D1 :

a 32 kDa protein component of the PS II reaction center, psbA.gene product

D2 :

a 34 kDa protein component of the PS II reaction center, psbD gene product

FR:

lar-red illumination

Lexpo and Lstat:

cells from lactate culture samples at exponential and stationary phase of growth

MV:

methylviologen

pBQ:

parabenzoquinone

PQ:

plastoquinone

PS II:

photosystem II

QA :

primary quinone electron acceptor

QB :

secondary quinone electron acceptor

TL:

thermoluminescence

References

  • BabcockGT and SauerK (1973) Electron paramagnetic resonance signal II in Spinach chloroplasts. I. Kinetic analysis for untreated chloroplasts. Biochim Biophys Acta 325: 483–503

    Google Scholar 

  • BennounP (1982) Evidence for a respiratory chain in chloroplasts. Proc Natl Acad Sci USA 79: 4352–4356

    Google Scholar 

  • BriantaisJM, DucruetJM, HodgesM and KrauseGH (1992) Effects of high light at chilling temperature on Photosystem II in spinach leaves. Photosynth Res 31: 1–10

    Google Scholar 

  • CalvayracR (1970) Relations entre les substrats, la respiration et la structure mitochondriale chez Euglena gracilis. Arch Mikrobiol 73: 308–314

    Google Scholar 

  • CalvayracR, LedoigtG and DubertretG (1975) Changements affectant la composition macromoléculaire du plastidome d' Euglena gracilis Z, au cours de la croissance hétérotrophe. Plant Sci Lett 5: 365–374

    Google Scholar 

  • CramerM and MyersJ (1952) Growth and photosynthetic characterization of Euglena gracilis. Arch Mikrobiol 17: 384–402

    Google Scholar 

  • DemeterS and Govindjee (1989) Thermoluminescence in plants. Physiol Plant 75: 121–130

    Google Scholar 

  • DemeterS, VassI, HidegE and SallaiA (1985) Comparative thermolumineseence study of triazine-resistant and-susceptible biotypes of Erigeron canadensis L. Biochim Biophys Acta 806: 16–24

    Google Scholar 

  • DesaiTS, SanePV and TatakeVG (1975) Thermoluminescence studies on spinach leaves and Euglena. Photochem Photobiol 21: 345–350

    Google Scholar 

  • DinerBA (1977) Dependence of the deactivation reactions of Photosystem II on the redox state of plastoquinone pool A varied under anaerobic conditions. Equilibria on the acceptor side of Photosystem II. Biochim Biophys Acta 460: 247–258

    Google Scholar 

  • FarineauJ (1990) Photochemical alterations of Photosystem II induced by two different photoinhibitory treatments in isolated chloroplasts of pea. A thermoluminescence study. Biochim Biophys Acta 1016: 357–363

    Google Scholar 

  • GreenbaumE and MauzerallDC (1976) Oxygen yield per flash of Chlorella coupled to chemical oxidants under anacrobic conditions. Photochem Photobiol 23: 369–372

    Google Scholar 

  • MeunierPC and PopovicR (1990) Control of misses in oxygen evolution by the oxido-reduction state of plastoquinone in Dunaliella tertiolecta. Photosynth Res 23: 213–221

    Google Scholar 

  • OhadR, AdirN, KoikeH, KyleDJ and InoueY (1990) Mechanism of photoinhibition in vivo. A reversible light-induced conformational change of reaction center II is related to an irreversible modification of the D1 protein. J Biol Chem 265: 1972–1979

    Google Scholar 

  • RebeilléF and GansP (1988) Interaction between chloroplasts and mitochondria in microalgae. Role of glycolysis. Plant Physiol 88: 973–975

    Google Scholar 

  • RutherfordAW (1989) Photosystem II, the water splitting enzyme. Trends Biochem Sci 14: 227–232

    Google Scholar 

  • RutherfordAW, CroftsAR and InoueY (1982) Thermoluminescence as a probe of Photosystem II photochemistry. The origin of the flash-induced glow peaks. Biochim Biophys Acta 682: 457–465

    Google Scholar 

  • RutherfordAW, Govindjee and InoueY (1984a) Charge accumulation and photochemistry in leaves studied by thermoluminescence and delayed light emission. Proc Natl Acad Sci USA 81: 1107–1111

    Google Scholar 

  • RutherfordAW, RengerG, KoikeH and InoueY (1984b) 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 

  • SanePV and RutherfordAW (1986) Thermoluminescence from photosynthetic membranes. In: Govindjee, AmeszJ and ForkDC (eds) Light Emission by Emission by Plants and Bacteria, pp 329–360. Academic Press, New York

    Google Scholar 

  • SanePV, DesaiTS, TatakeVG and Govindjee (1977) On the origin of glow peaks in Euglena cells, spinach chloroplasts and subchloroplast fragments enriched in System I or II. Photochem Photobiol 26: 33–39

    Google Scholar 

  • SchmidGH and ThibaultP (1983) Studies on the S-state distribution in Euglena gracilis. Z. Naturforsch 38c: 60–66

    Google Scholar 

  • TrebstA (1986) The topology of the plastoquinone and herbicide binding peptides of Photosystem II in the thylacoid membrane. Z Naturforsch 41c: 240–245

    Google Scholar 

  • Van BestJA and DuysensNM (1975) Reactions between primary and secondary acceptors of Photosystem II in Chlorelia pyrenoidosa under anaerobic conditions as studied by chlorophyll a fluorescence. Biochim Biophys Acta 408: 154–163

    Google Scholar 

  • Vass I and Inoue Y (1991) Thermoluminesence in the study of Photosystem II. In: Barber J (ed) Topics in Photosynthesis. The Photosystems. Elsevier Science Publishers, in press

  • VassI, DeakZ, DemeterS and HidegE (1990) Charge equilibrium between the water-oxidizing complex and donor D in Photosystem II. In: BaltscheffskyM (ed) Current Research in Photosynthesis, Vol 1, pp 809–812. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • VassI, HorvathG, HerczegT and DemeterS (1981) Photosynthetic energy conservation investigated by thermoluminescence. Activation energies and half-lives of thermoluminescence bands of chloroplasts determined by mathematical resolution of glow curves. Biochim Biophys Acta 634: 140–152

    Google Scholar 

  • VelthuysBR and VisserJWM (1975) The reactivation of EPR signal II in chloroplasts treated with reduced dichlorophenol-indophenol: evidence against a dark-equilibrium between two oxidation states of the oxygen evolving systems. FEBS Lett 55 109–112

    Google Scholar 

  • VermaasWFJ, RengerG and DohntG (1984) The reduction of the oxygen-evolving system in chloroplasts by thylakoid components. Biochim Biophys Acta 754: 194–202

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Farineau, J., Laval-Martin, D. Oxygen-evolving system and secondary quinonic acceptors are highly reduced in dark adapted Euglena cells: A thermoluminescence study. Photosynth Res 32, 167–180 (1992). https://doi.org/10.1007/BF00034793

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00034793

Key words

Navigation