Journal of Bioenergetics and Biomembranes

, Volume 45, Issue 1–2, pp 37–45 | Cite as

Effects of far-red light on fluorescence induction in infiltrated pea leaves under diminished ΔpH and Δφ components of the proton motive force

  • Alexander A. Bulychev
  • Vladimir A. Osipov
  • Dmitrii N. Matorin
  • Wim J. Vredenberg
Article

Abstract

Chlorophyll fluorescence induction curves induced by an actinic pulse of red light follow different kinetics in dark-adapted plant leaves and leaves preilluminated with far-red light. This influence of far-red light was abolished in leaves infiltrated with valinomycin known to eliminate the electrical (Δφ) component of the proton-motive force and was strongly enhanced in leaves infiltrated with nigericin that abolishes the ΔpH component. The supposed influence of ionophores on different components of the proton motive force was supported by differential effects of these ionophores on the induction curves of the millisecond component of chlorophyll delayed fluorescence. Comparison of fluorescence induction curves with the kinetics of P700 oxidation in the absence and presence of ionophores suggests that valinomycin facilitates a build-up of a rate-limiting step for electron transport at the site of plastoquinone oxidation, whereas nigericin effectively removes limitations at this site. Far-red light was found to be a particularly effective modulator of electron flows in chloroplasts in the absence of ΔpH backpressure on operation of the electron-transport chain.

Keywords

Infiltrated leaves Thylakoid membrane Proton motive force Ionophores Chlorophyll fluorescence P700 redox transients 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8:15–19CrossRefGoogle Scholar
  2. Altea F, Stengel A, Benza JP, Petersena E, Soll J, Groll M, Bölter B (2010) Ferredoxin:NADPH oxidoreductase is recruited to thylakoids by binding to a polyproline type II helix in a pH-dependent manner. Proc Natl Acad Sci USA 107:19260–19265CrossRefGoogle Scholar
  3. Baker NR, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ 30:1107–1125CrossRefGoogle Scholar
  4. Braun NA, Davis AW, Theg SM (2007) The chloroplast Tat pathway utilizes the transmembrane electric potential as an energy source. Biophys J 93:1993–1998CrossRefGoogle Scholar
  5. Buchta J, Grabolle M, Dau H (2007) Photosynthetic dioxygen formation studied by time-resolved delayed fluorescence measurements. Biochim Biophys Acta 1767:565–574CrossRefGoogle Scholar
  6. Bulychev AA (1984) Different kinetics of membrane potential formation in dark-adapted and preilluminated chloroplasts. Biochim Biophys Acta 766:647–652CrossRefGoogle Scholar
  7. Bulychev AA (2011) Induction changes in photosystems I and II in plant leaves upon modulation of membrane ion transport. Biochem (Mosc) Suppl Ser A Membr Cell Biol 5:335–342CrossRefGoogle Scholar
  8. Bulychev AA, Vredenberg WJ (2001) Modulation of photosystem II chlorophyll fluorescence by electrogenic events generated by photosystem I. Bioelectrochemistry 54:157–168CrossRefGoogle Scholar
  9. Bulychev AA, Vredenberg WJ (2010) Induction kinetics of photosystem I-activated P700 oxidation in plant leaves and their dependence on pre-energization. Russ J Plant Physiol 57:599–608CrossRefGoogle Scholar
  10. Bulychev AA, Niyazova MM, Turovetsky VB (1985) Evidence for the delayed photoactivation of electrogenic electron transport in chloroplast membranes. Biochim Biophys Acta 808:186–191CrossRefGoogle Scholar
  11. Dau H, Sauer K (1991) Electric field effect on chlorophyll fluorescence and its relation to Photosystem II charge separation reactions studied by a salt-jump tecgnique. Biochim Biophys Acta 1098:49–60CrossRefGoogle Scholar
  12. Dilley RA (1991) Energy coupling in chloroplasts: a calcium-gated switch controls proton fluxes between localized and delocalized proton gradients. Curr Topics Bioenerg 16:265–318CrossRefGoogle Scholar
  13. Feild TS, Nedbal L, Ort DR (1998) Nonphotochemical reduction of the plastoquinone pool in sunflower leaves originates from chlororespiration. Plant Physiol 116:1209–1218CrossRefGoogle Scholar
  14. Foyer C, Furbank R, Harbinson J, Horton P (1990) The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves. Photosynth Res 25:83–100CrossRefGoogle Scholar
  15. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63:1637–1661CrossRefGoogle Scholar
  16. Goltsev V, Zaharieva I, Chernev P, Strasser RJ (2009) Delayed fluorescence in photosynthesis. Photosynth Res 101:217–232CrossRefGoogle Scholar
  17. Johnson MP, Ruban AV (2011) Restoration of rapidly reversible photoprotective energy dissipation in the absence of PsbS protein by enhanced ΔpH. J Biol Chem 286:19973–19981CrossRefGoogle Scholar
  18. Johnson MP, Zia A, Ruban AV (2012) Elevated ΔpH restores rapidly reversible photoprotective energy dissipation in Arabidopsis chloroplasts deficient in lutein and xanthophyll cycle activity. Planta 235:193–204CrossRefGoogle Scholar
  19. Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci USA 108:13317–13322CrossRefGoogle Scholar
  20. Joly D, Jemâa E, Carpentier R (2010) Redox state of the photosynthetic electron transport chain in wild-type and mutant leaves of Arabidopsis thaliana: impact on photosystem II fluorescence. J Photochem Photobiol B Biol 98:180–187CrossRefGoogle Scholar
  21. Karlish SJD, Avron M (1971) Energy transfer inhibition and ion movements in isolated chloroplasts. Eur J Biochem 20:51–57CrossRefGoogle Scholar
  22. Katona E, Neimanis S, Schönknecht G, Heber U (1992) Photosystem I-dependent cyclic electron transport is important in controlling Photosystem II activity in leaves under conditions of water stress. Photosynth Res 34:449–464CrossRefGoogle Scholar
  23. Kramer DM, Crofts AR (1996) Control and measurement of photosynthetic transport in vivo. In: Baker NR (ed) Photosynthesis and environment. Springer, Dordrecht, pp 25–66Google Scholar
  24. Kramer DM, Avenson TJ, Edwards GE (2004) Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci 9:349–357CrossRefGoogle Scholar
  25. Lazar D, Schansker G (2009) Models of chlorophyll a fluorescence transents. In: Laisk A, Nedbal L, Govindjee (eds) Photosynthesis in silico. Springer, Dordrecht, pp 85–123CrossRefGoogle Scholar
  26. Nixon PJ, Rich PR (2006) Chlororespiratory pathways and their physiological significance. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, Dordrecht, pp 237–251CrossRefGoogle Scholar
  27. Renger G (1972) The action of 2-anilinothiophenes as accelerators of the deactivation reactions in the water-splitting enzyme system of photosynthesis. Biochim Biophys Acta 256:428–439CrossRefGoogle Scholar
  28. Satoh K (1982) Mechanism of photoactivation of electron transport in intact Bryopsis chloroplasts. Plant Physiol 70:1413–1416CrossRefGoogle Scholar
  29. Schansker G, Strasser RJ (2005) Quantification of non-QB-reducing centers in leaves using a far-red pre-illumination. Photosynth Res 84:145–151CrossRefGoogle Scholar
  30. 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 1797:1313–1326CrossRefGoogle Scholar
  31. Tyystjarvi E, Vass I (2004) Light emission as a probe of charge separation and recombination in the photosynthetic apparatus: Relation of prompt fluorescence to delayed light emission and thermoluminescence. In: Papageorgiou G (ed) Chlorophyll fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 363–388CrossRefGoogle Scholar
  32. Voorthuysen T, Bulychev AA, Dassen JНА, Snel JFH, Vredenberg WJ (1996) Suppression of flash-induced PSII-dependent electrogenesis caused by proton pumping in chloroplasts. Physiol Plant 98:156–164CrossRefGoogle Scholar
  33. Vredenberg WJ (2011) Kinetic analyses and mathematical modeling of primary photochemical and photoelectrochemical processes in plant photosystems. Biosystems 103:138–151CrossRefGoogle Scholar
  34. Vredenberg WJ, Bulychev AA (1976) Changes in the electrical potential across the thylakoid membranes of illuminated intact chloroplast in the presence of membrane-modifying agents. Plant Sci Lett 7:101–107CrossRefGoogle Scholar
  35. Vredenberg WJ, Bulychev AA (2003) Photoelectric effects on chlorophyll fluorescence of photosystem II in vivo. Kinetics in the absence and presence of valinomycin. Bioelectrochemistry 60:87–95CrossRefGoogle Scholar
  36. Vredenberg WJ, Bulychev AA (2010) Photoelectrochemical control of the balance between cyclic- and linear electron transport in photosystem I. Algorithm for P700+ induction kinetics. Biochim Biophys Acta 1797:1521–1532CrossRefGoogle Scholar
  37. Vredenberg W, Durchan M, Prasil O (2007) On the chlorophyll a fluorescence yield in chloroplasts upon excitation with twin turnover flashes (TTF) and high frequency flash trains. Photosynth Res 93:183–192CrossRefGoogle Scholar
  38. Vredenberg W, Durchan M, Prášil O (2009) Photochemical and photoelectrochemical quenching of chlorophyll fluorescence in photosystem II. Biochim Biophys Acta 1787:1468–1478CrossRefGoogle Scholar
  39. Wraight CA, Crofts AR (1971) Delayed fluorescence and the high-energy state of chloroplasts. Eur J Biochem 19:386–397CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Alexander A. Bulychev
    • 1
  • Vladimir A. Osipov
    • 1
  • Dmitrii N. Matorin
    • 1
  • Wim J. Vredenberg
    • 2
  1. 1.Department of Biophysics, Faculty of BiologyMoscow State UniversityMoscowRussia
  2. 2.Laboratory of Plant PhysiologyWageningen University and ResearchWageningenThe Netherlands

Personalised recommendations