Photosynthesis Research

, Volume 98, Issue 1–3, pp 189–197

Characterization of the secondary electron-transfer pathway intermediates of photosystem II containing low-potential cytochrome b559

Regular Paper

Abstract

β-carotene (Car) and chlorophyll (Chl) function as secondary electron donors in photosystem II (PS II) under conditions, such as low temperature, when electron donation from the O2-evolving complex is inhibited. In prior studies of the formation and decay of Car•+ and Chl•+ species at low temperatures, cytochrome b559 (Cyt b559) was chemically oxidized prior to freezing the sample. In this study, the photochemical formation of Car•+ and Chl•+ is characterized at low temperature in O2-evolving Synechocystis PS II treated with ascorbate to reduce most of the Cyt b559. Not all of the Cyt b559 is reduced by ascorbate; the remainder of the PS II reaction centers, containing oxidized low-potential Cyt b559, give rise to Car•+ and Chl•+ species after illumination at low temperature that are characterized by near-IR spectroscopy. These data are compared to the measurements on ferricyanide-treated O2-evolving Synechocystis PS II in which the Car•+ and Chl•+ species are generated in PS II centers containing mostly high- and intermediate-potential Cyt b559. Spectral differences observed in the ascorbate-reduced PS II samples include decreased intensity of the Chl•+ and Car•+ absorbance peaks, shifts in the Car•+ absorbance maxima, and lack of formation of a 750 nm species that is assigned to a Car neutral radical. These results suggest that different spectral forms of Car are oxidized in PS II samples containing different redox forms of Cyt b559, which implies that different secondary electron donors are favored depending on the redox form of Cyt b559 in PS II.

Keywords

Carotenoid radical cation Chlorophyll radical cation Cytochrome b559 Photosystem II 

Abbreviations

β-DM

β-Dodecylmaltoside

Car

β-Carotene

Chl

Monomeric chlorophyll

Car•+

β-Carotene radical cation

Car

β-Carotene neutral radical

Chl•+

Chlorophyll radical cation

CP43

Chlorophyll-binding protein encoded by psbC

CP47

Chlorophyll-binding protein encoded by psbB

Cyt b559

Cytochrome b559

D1

D1 polypeptide

D2

D2 polypeptide

HP

High potential

IP

Intermediate potential

LP

Low potential

MES

2-(N-Morpholino) ethane sulfonic acid

P680

Primary electron donor chlorophyll of PS II

PS II

Photosystem II

QA

Bound quinone electron acceptor

QB

Exchangeable quinone electron acceptor of PS II

RC

Reaction center

Supplementary material

11120_2008_9360_MOESM1_ESM.doc (358 kb)
(DOC 358 kb)

References

  1. Bautista JA, Tracewell CA, Schlodder E, Cunningham FX Jr, Brudvig GW, Diner BA (2005) Construction, characterization of genetically modified Synechocystis sp. PCC 6803 photosystem II core complexes containing carotenoids with shorter π-conjugation than β-carotene. J Biol Chem 280:38839–38850. doi:10.1074/jbc.M504953200 PubMedCrossRefGoogle Scholar
  2. Berthomieu C, Boussac A, Mantele W, Breton J, Nabedryk E (1992) Molecular changes following oxidoreduction of cytochrome b 559 characterized by Fourier transform infrared difference spectroscopy and electron paramagnetic resonance: photooxidation in photosystem II and electrochemistry of isolated cytochrome b 559 and iron protoporphyrin IX-bisimidazole model compounds. Biochemistry 31:11460–11471. doi:10.1021/bi00161a026 PubMedCrossRefGoogle Scholar
  3. Buser CA, Thompson LK, Diner BA, Brudvig GW (1990) Electron-transfer reactions in manganese-depleted photosystem II. Biochemistry 29:8977–8985. doi:10.1021/bi00490a014 PubMedCrossRefGoogle Scholar
  4. Buser CA, Diner BA, Brudvig GW (1992) Photooxidation of cytochrome b 559 in oxygen-evolving photosystem II. Biochemistry 31:11449–11459. doi:10.1021/bi00161a025 PubMedCrossRefGoogle Scholar
  5. Cramer WA, Whitmarsh J (1977) Photosynthetic cytochromes. Annu Rev Plant Physiol 28:133–172. doi:10.1146/annurev.pp.28.060177.001025 CrossRefGoogle Scholar
  6. De Las Rivas J, Klein J, Barber J (1995) pH sensitivity of the redox state of cytochrome b 559 may regulate its function as a protectant against donor and acceptor. Photosynth Res 46:193–202. doi:10.1007/BF00020430 CrossRefGoogle Scholar
  7. Erixon K, Butler WL (1971) The relationship between Q, C-550 and cytochrome b 559 in photoreactions at −196 degrees in chloroplasts. Biochim Biophys Acta 234:381–389. doi:10.1016/0005-2728(71)90205-2 PubMedCrossRefGoogle Scholar
  8. Gao Y, Shinopoulos KE, Tracewell CA, Focsan AL, Brudvig GW, Kispert LD (2008) Formation of carotenoid neutral radicals in photosystem II. J Phys Chem B (submitted)Google Scholar
  9. Hanley J, Deligiannakis Y, Pascal A, Faller P, Rutherford AW (1999) Carotenoid oxidation in photosystem II. Biochemistry 38:8189–8195. doi:10.1021/bi990633u PubMedCrossRefGoogle Scholar
  10. Holzwarth AR, Muller MG, Reus M, Nowaczyk M, Sander J, Rogner M (2006) Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: pheophytin is the primary electron acceptor. Proc Natl Acad Sci USA 103:6895–6900. doi:10.1073/pnas.0505371103 PubMedCrossRefGoogle Scholar
  11. Kaminskaya O, Kurreck J, Irrgang KD, Renger G, Shuvalov VA (1999) Redox and spectral properties of cytochrome b 559 in different preparations of photosystem II. Biochemistry 38:16223–16235. doi:10.1021/bi991257g PubMedCrossRefGoogle Scholar
  12. Kaminskaya O, Kern J, Shuvalov VA, Renger G (2005) Extinction coefficients of cytochromes b 559 and c 550 of Thermosynechococcus elongatus and Cyt b 559 /PS II stoichiometry of higher plants. Biochim Biophys Acta 1708:333–341. doi:10.1016/j.bbabio.2005.05.002 PubMedCrossRefGoogle Scholar
  13. Kaminskaya O, Shuvalov VA, Renger G (2007) Evidence for a novel quinone-binding site in the photosystem II (PS II) complex that regulates the redox potential of cytochrome b 559. Biochemistry 46:1091–1105. doi:10.1021/bi0613022 PubMedCrossRefGoogle Scholar
  14. Lakshmi KV, Reifler MJ, Chisholm DA, Wang JY, Diner BA, Brudvig GW (2002) Correlation of the cytochrome c 550 content of cyanobacterial photosystem II with the EPR properties of the oxygen-evolving complex. Photosynth Res 72:175–189. doi:10.1023/A:1016140902662 PubMedCrossRefGoogle Scholar
  15. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II. Nature 438:1040–1044. doi:10.1038/nature04224 PubMedCrossRefGoogle Scholar
  16. Magnuson A, Rova M, Mamedov F, Fredriksson PO, Styring S (1999) The role of cytochrome b 559 and tyrosineD in protection against photoinhibition during in vivo photoactivation of photosystem II. Biochim Biophys Acta 1411:180–191. doi:10.1016/S0005-2728(99)00044-4 PubMedCrossRefGoogle Scholar
  17. Mamedov F, Gadjieva R, Styring S (2007) Oxygen-induced changes in the redox state of the cytochrome b 559 in photosystem II depend on the integrity of the Mn cluster. Physiol Plant 131:41–49. doi:10.1111/j.1399-3054.2007.00938.x PubMedCrossRefGoogle Scholar
  18. Roncel M, Boussac A, Zurita JL, Bottin H, Sugiura M, Kirilovsky D et al (2003) Redox properties of the photosystem II cytochromes b 559 and c 550 in the cyanobacterium Thermosynechococcus elongatus. J Biol Inorg Chem 8:206–216. doi:10.1007/s00775-002-0406-7 PubMedCrossRefGoogle Scholar
  19. Schweitzer RH, Brudvig GW (1997) Fluorescence quenching by chlorophyll cations in photosystem II. Biochemistry 36:11351–11359. doi:10.1021/bi9709203 PubMedCrossRefGoogle Scholar
  20. Shibamoto T, Kato Y, Watanabe T (2008) Spectroelectrochemistry of cytochrome b 559 in the D1-D2-Cyt b 559 complex from spinach. FEBS Lett 582:1490–1494. doi:10.1016/j.febslet.2008.03.041 PubMedCrossRefGoogle Scholar
  21. Stewart DH (1998) Characterization of redox centers in photosystem II. Ph.D. Thesis, Yale UniversityGoogle Scholar
  22. Stewart DH, Brudvig GW (1998a) Cytochrome b 559 of photosystem II. Biochim Biophys Acta 1367:63–87. doi:10.1016/S0005-2728(98)00139-X PubMedCrossRefGoogle Scholar
  23. Stewart DH, Brudvig GW (1998b) A new model of cytochrome b 559 function based on the observation of a reversible redox-linked interconversion between two redox forms of cytochrome b 559. In: Garab G (ed) Photosynthesis mechanism and effects, vol 2. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 1113–1116Google Scholar
  24. Thompson LK, Miller AF, Buser CA, de Paula JC, Brudvig GW (1989) Characterization of the multiple forms of cytochrome b 559 in photosystem II. Biochemistry 28:8048–8056. doi:10.1021/bi00446a012 PubMedCrossRefGoogle Scholar
  25. Tracewell CA, Brudvig GW (2003) Two redox-active β-carotene molecules in photosystem II. Biochemistry 42:9127–9136. doi:10.1021/bi0345844 PubMedCrossRefGoogle Scholar
  26. Tracewell CA, Brudvig GW (2008) Photooxidation of multiple chlorophylls occurs via the secondary electron transfer pathways of oxygen-evolving photosystem II. Biochemistry (submitted)Google Scholar
  27. Tracewell CA, Cua A, Stewart DH, Bocian DF, Brudvig GW (2001) Characterization of carotenoid and chlorophyll photooxidation in photosystem II. Biochemistry 40:193–203. doi:10.1021/bi001992o PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Department of ChemistryYale UniversityNew HavenUSA
  2. 2.Division of Chemistry and Chemical EngineeringCalifornia Institute of TechnologyPasadenaUSA

Personalised recommendations