Skip to main content
Log in

Low-temperature (77 K) phosphorescence of triplet chlorophyll in isolated reaction centers of photosystem II

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

Abstract

Phosphorescence characterized by the main emission band at 952 ± 1 nm (1.30 eV), the lifetime of 1.5 ± 0.1 ms and the quantum yield nearly equal to that for monomeric chlorophyll a in aqueous detergent dispersions, has been detected in isolated reaction centers (RCs) of spinach photosystem II at 77 K. The excitation spectrum shows maxima corresponding to absorption bands of chlorophyll a, pheophytin a, and β-carotene. The phosphorescence intensity strongly depends upon the redox state of RCs. The data suggest that the phosphorescence signal originates from the chlorophyll triplet state populated via charge recombination in the radical pair \({\rm P}_{680}^{+}{\rm Pheo}_{{\rm D}1}^{-}.\)

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

Similar content being viewed by others

Abbreviations

BTS buffer:

20 mM Bis–Tris (pH 6.5)/20 mM MgCl2/5 mM CaCl2/0.03 % (w/v) n-dodecyl-β-D-maltoside/100 mM MgSO4/200 mM sucrose

Chl:

Chlorophyll a

ChlD1 :

Monomeric Chl at the active cofactor branch

cyt b559:

Cytochrome b559

β-car:

β-Carotene

D1 and D2:

The D1 and D2 polypeptides of the reaction center

Pheo:

Pheophytin a

PheoD1 :

Pheo at the active cofactor branch

PSII:

Photosystem II

P680 :

A dimer of Chl molecules

RC:

Reaction center

SiMo:

Silicomolybdate

References

  • Angerhofer A, Friso G, Giacometti GM, Carbonera D, Giacometti G (1994) Optically detected magnetic resonance study on the origin of the pheophytin triplet state in D1/D2-cytochrome b-559 complexes. Biochim Biophys Acta 1188:35–45

    Article  CAS  Google Scholar 

  • Carbonera D, Giacometti G, Agostini G (1994) A well resolved ODMR triplet minus singlet spectrum of P680 from PSII particles. FEBS Lett 343:200–204

    Article  CAS  PubMed  Google Scholar 

  • Danielius RV, Satoh K, van Kan PJM, Plijter JJ, Nuijs AM, van Gorkom HJ (1987) The primary reaction of photosystem II in the D1-D2-cytochrome b-559 complex. FEBS Lett 213:241–244

  • Diner BA, Schlodder E, Nixon PJ, Coleman WJ, Rappaport F, Lavergne J, Vermaas WFJ, Chisholm DA (2001) Site-directed mutations at D1-His198 and D2-His197 of photosystem II in Synechocystis PCC 6803: sites of primary charge separation and cation and triplet stabilization. Biochemistry 40:9265–9281

    Article  CAS  PubMed  Google Scholar 

  • Durrant JR, Giorgi LB, Barber J, Klug DR, Porter G (1990) Characterisation of triplet states in isolated photosystem II reaction centres: oxygen quenching as a mechanism for photodamage. Biochim Biophys Acta 1017:167–175

    Article  CAS  Google Scholar 

  • Dvornikov SS, Knyukshto VN, Solovyov KN, Tsvirko MP (1979) Phosphorescence of chlorophylls a and b and their pheophytins. Opt Spekt (URSS) 46:689–695

    CAS  Google Scholar 

  • Germano M, Shkuropatov AY, Permentier H, de Wijn R, Hoff AJ, Shuvalov VA, van Gorkom HJ (2001) Pigment organization and their interactions in reaction centers of photosystem II: optical spectroscopy at 6 K of reaction centers with modified pheophytin composition. Biochemistry 40:11472–11482

    Article  CAS  PubMed  Google Scholar 

  • Groot M-L, Peterman EJG, van Kan PJM, van Stokkum IHM, Dekker JP, van Grondelle R (1994) Temperature-dependent triplet and fluorescence quantum yields of the photosystem II reaction center described in a thermodynamic model. Biophys J 67:318–330

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hanson Ö, Mathis P, Satoh K (1987) Magnetic field effects on the primary reactions in photosystem II. In: Baltscheffsky M (ed) Current research in photosynthesis, vol I. Kluwer, Dordrecht, pp 439–442

    Google Scholar 

  • Hartzler DA, Niedzwiedzki DM, Bryant DA, Blankenship RE, Pushkar Y, Savikhin S (2014) Triplet excited state energies and phosphorescence spectra of (bacterio)chlorophylls. J Phys Chem 118:7221–7232

  • Klimov VV, Klevanik AV, Shuvalov VA, Krasnovsky AA (1977) Reduction of pheophytin in the primary light reaction of photosystem II. FEBS Lett 82:183–186

    Article  CAS  PubMed  Google Scholar 

  • Konermann L, Yruela I, Holzwarth AR (1997) Pigment assignment in the absorption spectrum of the photosystem II reaction center by site-selection fluorescence spectroscopy. Biochemistry 36:7498–7502

    Article  CAS  PubMed  Google Scholar 

  • Krasnovsky AA Jr (1979) Photoluminescence of singlet oxygen in pigment solutions. Photochem Photobiol 29:29–36

    Article  CAS  Google Scholar 

  • Krasnovsky AA Jr (1982) Delayed fluorescence and phosphorescence of plant pigments. Photochem Photobiol 36:733–741

    Article  Google Scholar 

  • Krasnovsky AA Jr (1994) Singlet oxygen and primary mechanisms of photooxidative damage of chloroplasts. Studies based on detection of oxygen and pigment phosphorescence. Proc Roy Soc 102B:219–235

    Google Scholar 

  • Krasnovsky AA Jr (2014) Phosphorescence of triplet chlorophylls. In: Kadish K, Smith KM, Guilard R (eds) Handbook of porphyrin science, vol 33. World Scientific Publishing, Singapore, pp 78–165

  • Krasnovsky AA Jr, Kovalev YV (2014) Spectral and kinetic parameters of phosphorescence of triplet chlorophyll a in the photosynthetic apparatus of plants. Biochemistry (Moscow) 79:349–361

    Article  CAS  Google Scholar 

  • Krasnovsky AA Jr, Lebedev NN, Litvin FF (1977) Phosphorescence and delayed fluorescence of chlorophyll and its precursors in solutions, leaves and chloroplasts. Studia Biophys 65:81–89

    Google Scholar 

  • Krasnovsky AA Jr, Neverov KV, Egorov SYu, Roeder B, Levald T (1990) Photophysical studies of pheophorbide a and pheophytin a. Phosphorescence and photosensitized singlet oxygen luminescence. J Photochem Photobiol B 5:245–254

    Article  PubMed  Google Scholar 

  • Kwa SLS, Newell WR, van Grondelle R, Dekker JP (1992) The reaction center of photosystem II studied with polarized fluorescence spectroscopy. Biochim Biophys Acta 1099:193–202

    Article  CAS  Google Scholar 

  • Lubitz W (2002) Pulse EPR and ENDOR studies of light-induced radicals and triplet states in photosystem II of oxygenic photosynthesis. Phys Chem Chem Phys 4:5539–5545

    Article  CAS  Google Scholar 

  • Macpherson AN, Telfer A, Barber J, Truscott TG (1993) Direct detection of singlet oxygen from isolated photosystem II reaction centres. Biochim Biophys Acta 1143:301–309

    Article  CAS  Google Scholar 

  • Nanba O, Satoh K (1987) Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci USA 84:109–112

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Neverov KV, Krasnovsky AA Jr (2004) Phosphorescence analysis of the chlorophyll triplet states in preparations of photosystem II. Biophysics 49:469–474

    Google Scholar 

  • Neverov KV, Santabarbara S, Krasnovsky AA Jr (2011) Phosphorescence study of chlorophyll d photophysics. Determination of the energy and lifetime of the photo-excited triplet state. Evidence of singlet oxygen photosensitization. Photosynth Res 108:101–106

  • Noguchi T, Tomo T, Inoue Y (1998) Fourier transform infrared study of the cation radical of P680 in the photosystem II reaction center: evidence for charge delocalization on the chlorophyll dimer. Biochemistry 37:13614–13625

    Article  CAS  PubMed  Google Scholar 

  • Noguchi T, Tomo T, Kato C (2001) Triplet formation on a monomeric chlorophyll in the photosystem II reaction center as studied by time-resolved infrared spectroscopy. Biochemistry 40:2176–2185

    Article  CAS  PubMed  Google Scholar 

  • Nugent JHA, Telfer A, Demetriou C, Barber J (1989) Electron transfer in the isolated photosystem II reaction centre complex. FEBS Lett 255:53–58

    Article  CAS  Google Scholar 

  • Okamura MY, Satoh K, Isaacson RA, Feher G (1987) Evidence of the primary charge separation in the D1D2 complex of photosystem II from spinach: EPR of the triplet state. In: Biggins J (ed) Progress in photosynthesis research, vol I. Martinus Nijhoff Publishers, Dordrecht, pp 379–381

    Google Scholar 

  • Renger G, Holzwarth AR (2005) Primary electron transfer. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water/plastoquinone oxidoreductase. Springer, Dordrecht, pp 139–175

    Chapter  Google Scholar 

  • Satoh K (1993) Isolation and properties of the photosystem II reaction center. In: Deisenhofer J, Norris JR (eds) The photosynthetic reaction center, vol I. Academic Press, London, pp 289–318

    Chapter  Google Scholar 

  • Schlodder E, Renger T, Raszewski G, Coleman WJ, Nixon PJ, Cohen RO, Diner BA (2008) Site-directed mutations at D1-Thr 179 of photosystem II in Synechocystis sp. PCC 6803 modify the spectroscopic properties of the accessory chlorophyll in the D1-branch of the reaction center. Biochemistry 47:3143–3154

    Article  CAS  PubMed  Google Scholar 

  • Takahashi Y, Hansson Ö, Mathis P, Satoh K (1987) Primary radical pair in the Photosystem II reaction centre. Biophys Biochim Acta 893:49–59

  • Takahashi Y, Satoh K, Itoh S (1989) Silicomolybdate substitutes for the function of a primary electron acceptor and stabilizes charge separation in the photosystem II reaction center complex. FEBS Lett 255:133–138

    Article  CAS  Google Scholar 

  • Takiff L, Boxer SG (1988a) Phosphorescence spectra of bacteriochlorophylls. J Am Chem Soc 110:4425–4426

    Article  CAS  Google Scholar 

  • Takiff L, Boxer SG (1988b) Phosphorescence from the primary electron donor in Rhodobacter sphaeroides and Rhodopseudomonas viridis reaction centers. Biochim Biophys Acta 932:325–334

    Article  CAS  Google Scholar 

  • van der Vos R, van Leeuwen PJ, Braun P, Hoff AJ (1992) Analysis of the optical absorbance spectra of D1-D2-cytochrome b-559 complexes by absorbance-detected magnetic resonance: structural properties of P680. Biophys Biochim Acta 1140:184–198

    Article  Google Scholar 

  • van Dorssen RJ, Breton J, Plijter JJ, Satoh K, van Gorkom HJ, Amesz J (1987) Spectroscopic properties of the reaction center and of the 47 kDa chlorophyll protein of photosystem II. Biochim Biophys Acta 893:267–274

    Article  Google Scholar 

  • van Kan PJM, Otte SCM, Kleinherenbrink FAM, Nieveen MC, Aartsma TJ, van Gorkom HJ (1990) Time-resolved spectroscopy at 10 K of the photosystem II reaction center; deconvolution of the red absorption band. Biochim Biophys Acta 1020:146–152

    Article  Google Scholar 

  • van Leeuwen PJ, Nieveen MC, van de Meent EJ, Dekker JP, van Gorkom HJ (1991) Rapid and simple isolation of pure photosystem II core and reaction center particles from spinach. Photosynth Res 28:149–153

    Article  PubMed  Google Scholar 

  • van Mieghem FJE, Satoh K, Rutherford AW (1991) A chlorophyll tilted 30° relative to the membrane in the photosystem II reaction centre. Biochim Biophys Acta 1058:379–385

    Article  Google Scholar 

  • Volk M, Gilbert M, Rousseau G, Richter M, Ogrodnik A, Michel-Beyerle M-E (1993) Similarity of primary radical pair recombination in photosystem II and bacterial reaction centers. FEBS Lett 336:357–362

    Article  CAS  PubMed  Google Scholar 

  • Yruela I, van Kan PJM, Müller MG, Holzwarth AR (1994) Characterization of a D1-D2-cyt b-559 complex containing 4 Chl a/2 pheophytin a isolated with the use of MgSO4. FEBS Lett 339:25–30

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Russian Academy of Sciences (the Programs “Molecular and Cell Biology” and “The fundamentals of technologies of nanostructures and nanomaterials”), by the Russian Foundation for Basic Research (Grants 13-04-40297-H, 15-04-05500), and by the Program “Leading Scientific Schools” (SS-4771.2014.4).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anatoly Ya. Shkuropatov.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Neverov, K.V., Krasnovsky, A.A., Zabelin, A.A. et al. Low-temperature (77 K) phosphorescence of triplet chlorophyll in isolated reaction centers of photosystem II. Photosynth Res 125, 43–49 (2015). https://doi.org/10.1007/s11120-015-0105-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-015-0105-1

Keywords

Navigation