Skip to main content

Advertisement

Log in

The energy flux theory 35 years later: formulations and applications

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

Abstract

Several models have been proposed for the energetic behavior of the photosynthetic apparatus and a variety of experimental techniques are nowadays available to determine parameters that can quantify this behavior. The Energy Flux Theory (EFT) developed by Strasser 35 years ago provides a straightforward way to formulate any possible energetic communication between any complex arrangement of interconnected pigment systems and any energy transduction by these systems. We here revisit the EFT, starting from the basic general definitions and equations and presenting applications in formulating the energy distribution in photosystem (PS) II units with variable connectivity, as originally derived, where certain simplifications were adopted. We then proceed to the derivation of equations for a PSII model of higher complexity, which corresponds, from the formalistic point of view, to the later formulated and now broadly accepted exciton–radical-pair model. We also compare the formulations derived with the EFT with those obtained, by different approaches, in the classic papers on energetic connectivity. Moreover, we apply the EFT for the evaluation of the excitation energy distribution between PSII and PSI and the distinction between state transitions and PSII to PSI excitation energy migration. Our analysis demonstrates that the EFT is a powerful approach for the formulation of any possible model, at any complexity level, even of models that may be proposed in the future, with the advantage that any possible energetic communication or energy transduction can be easily formulated mathematically by trivial algebraic equations. Moreover, the biophysical parameters introduced by the EFT and applicable for any possible model can be linked with obtainable experimental signals, provided that the theoretical resolution of the model does not go beyond the experimental resolution.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15

Similar content being viewed by others

References

  • Allen JF (1992) How does protein phosphorylation regulate photosynthesis. Trends Biochm Sci 17:12–17

    Article  CAS  Google Scholar 

  • Allen JF (1995) Thylakoid protein phosphorylation, state-1-state-2 transitions, and photosystem stoichiometry adjustment—redox control at multiple levels of gene expression. Physiol Plantarum 93:196–205

    Article  CAS  Google Scholar 

  • Butler WL (1980) Energy transfer between photosystem II units in a connected package model of the photochemical apparatus of photosynthesis. Proc Natl Acad Sci USA 77:4697–4701

    Article  PubMed  CAS  Google Scholar 

  • Butler WL, Kitajima M (1975) Energy transfer between photosystem II and photosystem I in chloroplasts. Biochim Biophys Acta 396:72–85

    Article  PubMed  CAS  Google Scholar 

  • Butler WL, Strasser RJ (1977) Tripartite model for the photochemical apparatus of green plant photosynthesis. Proc Natl Acad Sci USA 74:3382–3385

    Article  PubMed  CAS  Google Scholar 

  • Clayton RK (1966) Relations between photochemistry and fluorescence in cells and extracts of photosynthetic bacteria. Photochem Photobiol 5:807–821

    Article  CAS  Google Scholar 

  • Clayton RK (1967) An analysis of the relations between fluorescence and photochemistry during photosynthesis. J Theor Biol 14:173–186

    Article  PubMed  CAS  Google Scholar 

  • Cleland RE, Melis A, Neale PJ (1986) Mechanism of photoinhibition: photochemical reaction center inactivation in system II of chloroplast. Photosynth Res 9:79–88

    Article  CAS  Google Scholar 

  • Duysens LNM, Sweers HE (1963) Mechanism of two photochemical reactions in algae as studied by means of fluorescence. In: Japanese Society of Plant Physiologists (ed) Studies on microalgae and photosynthetic bacteria. University of Tokyo Press, Tokyo, pp 353–372

    Google Scholar 

  • Emerson R, Arnold WA (1932a) A separation of the reactions in photosynthesis by means of intermittent light. J Gen Physiol 15:391–420

    Article  PubMed  CAS  Google Scholar 

  • Emerson R, Arnold WA (1932b) The photochemical reaction in photosynthesis. J Gen Physiol 16:191–205

    Article  PubMed  CAS  Google Scholar 

  • Gaffron H, Wohl K (1936) Zur theorie der assimilation. Naturwissenschaften 24:81–90

    Article  CAS  Google Scholar 

  • Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Gilmore A, Itoh S, Govindjee (2000) Global spectral-kinetic analysis of room temperature chlorophyll a fluorescence from light harvesting antenna mutants of barley. Phil Trans R Soc Lond B 335:1–14

    Google Scholar 

  • Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160

    Article  CAS  Google Scholar 

  • Hipkins MF (1978) Kinetic analysis of the chlorophyll fluorescence inductions from chloroplasts blocked with 3-(3,4-dichlorophenyl)-1,1-dimethyurea. Biochim Biophys Acta 502:514–523

    Article  PubMed  CAS  Google Scholar 

  • Joliot A, Joliot P (1964) Etude cinétique de la réaction photochimique libérant l’oxygène au cours de la photosynthèse. CR Acad Sci Paris 258:4622–4625

    CAS  Google Scholar 

  • Kautsky H, Hirsch A (1931) Neue Versuche zur Kohlensäureassimilation. Naturwissenschaften 19:964

    Article  CAS  Google Scholar 

  • Ke B (2001) Photosynthesis: photobiochemistry and photobiophysics. Advances in photosynthesis and respiration (Series ed, Govindjee), vol 10. Kluwer Academic Publishers, Dordrecht

  • Kitajima M, Butler WL (1975a) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105–115

    Article  PubMed  CAS  Google Scholar 

  • Kitajima M, Butler WL (1975b) Excitation spectra for photosystem I and photosystem II in chloroplasts and the spectral characteristics of the distribution of quanta between the two photosystems. Biochim Biophys Acta 408:297–305

    Article  PubMed  CAS  Google Scholar 

  • Krause GH, Somersalo S, Zumbusch E, Weyers B, Laasch H (1990) On the mechanism of photoinhibition in chloroplasts. Relationship between changes in fluorescence and activity of photosystem II. J Plant Physiol 136:472–479

    Article  CAS  Google Scholar 

  • Lavergne J, Trissl H-W (1995) Theory of fluorescence induction in photosystem II: derivation of analytical expressions in a model including exciton–radical-pair equilibrium and restricted energy transfer between photosynthetic units. Biophys J 68:2474–2492

    Article  PubMed  CAS  Google Scholar 

  • Ley AC, Butler WL (1977) The distribution of excitation energy between photosystem I and photosystem II in Porphyridium cruentum. In: Miyachi S, Katoh S, Fujita Y, Shibata K (eds) Special edition of plant and cell physiology. Japanese Society of Plant Physiologists, Tokyo, pp 33–46

    Google Scholar 

  • Lombard F, Strasser RJ (1984) Evidence for spill over changes during state-1 to state-2 transition in green leaves. In: Sybesma C (ed) Advances in photosynthesis research III. Martinus Nijhoff/Dr W Junk Publishers, The Hague, pp 271–274

    Chapter  Google Scholar 

  • Melis A, Homann PH (1976) Heterogeneity of the photochemical centers in system II of chloroplasts. Photochem Photobiol 23(5):343–350

    Article  PubMed  CAS  Google Scholar 

  • Montal M, Darszon A, Strasser RJ (1978) Rhodopsin and bacteriorhodopsin in model membranes. In: Dutton L, Scarper A, Leigh JS (eds) Frontiers in biology energetics, vol 2. Academic Press, New York, pp 1109–1118

    Chapter  Google Scholar 

  • Murata N (1969) Control of excitation transfer in photosynthesis. II. Magnesium ion-dependent distribution of excitation energy between two pigment systems in spinach chloroplasts. Biochim Biophys Acta 189:171–181

    Article  PubMed  CAS  Google Scholar 

  • Paillotin G (1976a) Capture frequency of excitations and energy transfer between photosynthetic units in the photosystem II. J Theor Biol 58:219–235

    Article  PubMed  CAS  Google Scholar 

  • Paillotin G (1976b) Movement of excitations in the photosynthetic domains of photosystem II. J Theor Biol 58:237–252

    Article  CAS  Google Scholar 

  • Paillotin G (1977) Organization of the photosynthetic pigments and transfer of excitation energy. In: Hall DO, Coombs J, Goodwin TW (eds) Photosynthesis ′77: proceedings of the fourth international congress on photosynthesis. The Biochemical Society, London, pp 33–44

    Google Scholar 

  • Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll a fluorescence: a signature of photosynthesis. In: Advances in photosynthesis and respiration (Series ed, Govindjee), vol 19. Springer, Dordrecht

  • Robinson GW (1967) Excitation transfer and trapping in photosynthesis. In: Energy conversion by the photosynthetic apparatus. Brookhaven symposia in biology, number 19. Brookhaven National Laboratory, Upton, pp 16–48

  • Satoh K, Strasser RJ, Butler WL (1976) A demonstration of energy transfer from photosystem II to photosystem I in chloroplasts. Biochim Biophys Acta 440:337–345

    Article  PubMed  Google Scholar 

  • Sorokin EM (1985) The induction curve of chlorophyll a fluorescence in DCMU-treated chloroplasts and its properties. Photobiochem Photobiophys 9:3–19

    CAS  Google Scholar 

  • Stirbet AD, Govindjee Strasser BJ, Strasser RJ (1998) Chlorophyll a fluorescence induction in higher plants: modeling and numerical simulation. J Theor Biol 193:131–151

    Article  CAS  Google Scholar 

  • Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP-test. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol 5. Kluwer Academic, The Netherlands, pp 977–980

    Google Scholar 

  • Strasser RJ (1978) The grouping model of plant photosynthesis. In: Akoyunoglou G, Argyroudi-Akoyunoglou JH (eds) Chloroplast development. Elsevier/North Holland Biomedical Press, Amsterdam, pp 513–524

    Google Scholar 

  • Strasser RJ (1980) Bacteriorhodopsin and its position in the blue light syndrome. In: Senger H (ed) The blue light syndrome. Springer, Berlin, pp 30–37

    Google Scholar 

  • Strasser RJ (1981) The grouping model of plant photosynthesis: heterogeneity of photosynthetic units in thylakoids. In: Akoyunoglou G (ed) Photosynthesis III. Structure and molecular organisation of the photosynthetic apparatus. Balaban International Science Services, Philadelphia, pp 727–737

    Google Scholar 

  • Strasser RJ (1984) The dynamics of the photoreduction of protochlorophyll(ide) into chlorophyll(ide). In: C. Sironval C, Brouers M (eds) Protochlorophyllide reduction and greening. Martinus Nijhoff/Dr W Junk Publishers, The Hague/Boston/Lancaster, pp 317–327

  • Strasser RJ (1986) Mono-, bi- and polypartite models in photosynthesis. Photosynt Res 10:255–276

    Article  CAS  Google Scholar 

  • Strasser RJ, Butler WL (1976) Energy transfer in the photochemical apparatus of flashed bean leaves. Biochim Biophys Acta 449:412–419

    Article  PubMed  CAS  Google Scholar 

  • Strasser RJ, Butler WL (1977a) Energy transfer and distribution of excitation energy in the photosynthetic apparatus of spinach chloroplasts. Biochim Biophys Acta 460:230–238

    Article  PubMed  CAS  Google Scholar 

  • Strasser RJ, Butler WL (1977b) The yield of energy transfer and the spectral distribution of excitation energy in the photochemical apparatus of flashed bean leaves. Biochim Biophys Acta 462:295–306

    Article  PubMed  CAS  Google Scholar 

  • Strasser RJ, Greppin H (1981) Primary reactions of photochemistry in higher plants. In: Akoyunoglou G (ed) Photosynthesis III. Structure and molecular organisation of the photosynthetic apparatus. Balaban International Science Services, Philadelphia, PA, pp 717–726

    Google Scholar 

  • Strasser RJ, Tsimilli-Michael M (1998) Activity and heterogeneity of PS II probed in vivo by the chlorophyll a fluorescence rise O-(K)-J-I-P. In: Garab G (ed) Photosynthesis: mechanisms and effects, vol 5. Kluwer Academic Publishers, Dordrecht, pp 4321–4324

    Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanism, regulation and adaptation. Taylor and Francis, London, pp 443–480

    Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration (Series ed, Govindjee) vol 19. Springer, Dordrecht, pp 321–362

  • Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta 1797:1313–1326

    Article  PubMed  CAS  Google Scholar 

  • Tsala G, Strasser RJ (1984) Energy distribution changes during phosphorylation of the light harvesting complex in thylakoids. In: Sybesma C (ed) Advances in photosynthesis research III. Martinus Nijhoff/Dr W Junk Publishers, The Hague, pp 279–282

    Chapter  Google Scholar 

  • Tsimilli-Michael M, Strasser RJ (2008) Experimental resolution and theoretical complexity determine the amount of information extractable from the chlorophyll fluorescence transient OJIP. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Photosynthesis. Energy from the sun. Springer, Dordrecht, pp 697–701

    Chapter  Google Scholar 

  • Tsimilli-Michael M, Pêcheux M, Strasser RJ (1999) Light and heat stress adaptation of the symbionts of temperate and coral reef foraminifers probed in hospite by the chlorophyll a fluorescence kinetics O-J-I-P. Z Naturforsch 54C:671–680

    Google Scholar 

  • Vredenberg WJ, Duysens LNM (1963) Transfer of energy from bacteriochlorophyll to a reaction centre during bacterial photosynthesis. Nature (London) 197:355–357

    Article  CAS  Google Scholar 

Download references

Acknowledgments

M T-M thanks Dr Pierre Haldimann for stimulating discussions, critical comments and valuable suggestions during the preparation of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Merope Tsimilli-Michael.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tsimilli-Michael, M., Strasser, R.J. The energy flux theory 35 years later: formulations and applications. Photosynth Res 117, 289–320 (2013). https://doi.org/10.1007/s11120-013-9895-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-013-9895-1

Keywords

Navigation