Photosynthesis Research

, Volume 124, Issue 3, pp 253–265 | Cite as

Critical assessment of the emission spectra of various photosystem II core complexes

  • Jinhai Chen
  • Adam Kell
  • Khem Acharya
  • Christopher Kupitz
  • Petra Fromme
  • Ryszard Jankowiak
Regular Paper


We evaluate low-temperature (low-T) emission spectra of photosystem II core complexes (PSII-cc) previously reported in the literature, which are compared with emission spectra of PSII-cc obtained in this work from spinach and for dissolved PSII crystals from Thermosynechococcus (T.) elongatus. This new spectral dataset is used to interpret data published on membrane PSII (PSII-m) fragments from spinach and Chlamydomonas reinhardtii, as well as PSII-cc from T. vulcanus and intentionally damaged PSII-cc from spinach. This study offers new insight into the assignment of emission spectra reported on PSII-cc from different organisms. Previously reported spectra are also compared with data obtained at different saturation levels of the lowest energy state(s) of spinach and T. elongatus PSII-cc via hole burning in order to provide more insight into emission from bleached and/or photodamaged complexes. We show that typical low-T emission spectra of PSII-cc (with closed RCs), in addition to the 695 nm fluorescence band assigned to the intact CP47 complex (Reppert et al. J Phys Chem B 114:11884–11898, 2010), can be contributed to by several emission bands, depending on sample quality. Possible contributions include (i) a band near 690–691 nm that is largely reversible upon temperature annealing, proving that the band originates from CP47 with a bleached low-energy state near 693 nm (Neupane et al. J Am Chem Soc 132:4214–4229, 2010; Reppert et al. J Phys Chem B 114:11884–11898, 2010); (ii) CP43 emission at 683.3 nm (not at 685 nm, i.e., the F685 band, as reported in the literature) (Dang et al. J Phys Chem B 112:9921–9933, 2008; Reppert et al. J Phys Chem B 112:9934–9947, 2008); (iii) trap emission from destabilized CP47 complexes near 691 nm (FT1) and 685 nm (FT2) (Neupane et al. J Am Chem Soc 132:4214–4229, 2010); and (iv) emission from the RC pigments near 686–687 nm. We suggest that recently reported emission of single PSII-cc complexes from T. elongatus may not represent intact complexes, while those obtained for T. elongatus presented in this work most likely represent intact PSII-cc, since they are nearly indistinguishable from emission spectra obtained for various PSII-m fragments.


Energy transfer Fluorescence Light-harvesting Photosynthesis Photosystem II 



Charge transfer




Excitation energy transfer




Hole burning


Nonphotochemical hole burning


Membrane photosystem II




Photosystem II


Photosystem II core complex


Reaction center







This work was supported by the Chemical Sciences, Geosciences, and Biosciences Division, Office of Basic Energy Sciences, Office of Science, U.S. Department of Energy (Award No. DE-SC0006678 to R.J.) and the Center for Bio-Inspired Solar Fuel Production, an Energy Frontier Research Center funded by the DOE, Office of Basic Energy Sciences (Award No. DE-SC0001016 to P.F.). R.J. acknowledges useful discussions with Dr. E. Krausz (Research School of Chemistry, Australian National University) over the years and PSII-cc samples from spinach. We also thank Dr. V. Zazubovich for discussions and critical reading of our manuscript.

Supplementary material

11120_2015_128_MOESM1_ESM.docx (467 kb)
Supplementary material 1 (DOCX 467 kb)


  1. Acharya K, Neupane B, Reppert M, Feng X, Jankowiak R (2010) On the unusual temperature-dependent emission of the CP47 antenna protein complex of photosystem II. J Phys Chem Lett 1:2310–2315CrossRefGoogle Scholar
  2. Acharya K, Neupane B, Zazubovich V, Sayre RT, Picorel R, Seibert M, Jankowiak R (2012a) Site energies of active and inactive pheophytins in the reaction center of photosystem II from Chlamydomonas reinhardtii. J Phys Chem B 116:3890–3899CrossRefPubMedGoogle Scholar
  3. Acharya K, Zazubovich V, Reppert M, Jankowiak R (2012b) Primary electron donor(s) in isolated reaction center of photosystem II from Chlamydomonas reinhardtii. J Phys Chem B 116:4860–4870CrossRefPubMedGoogle Scholar
  4. Andrizhiyevskaya EG, Chojnicka A, Bautista JA, Diner BA, van Grondelle R, Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II. Photosynth Res 84:173–180CrossRefPubMedGoogle Scholar
  5. Blankenship RE (2002) Molecular mechanisms of photosynthesis. Blackwell Science, OxfordCrossRefGoogle Scholar
  6. Brecht M, Skandary S, Hellmich J, Glöckner C, Konrad A, Hussels M, Meixner AJ, Zouni A, Schlodder E (2014) Spectroscopic properties of photosystem II core complexes from Thermosynechococcus elongatus revealed by single-molecule experiments. Biochim Biophys Acta 1837:773–781CrossRefPubMedGoogle Scholar
  7. Chang H-C, Jankowiak R, Yocum CF, Picorel R, Alfonso M, Seibert M, Small GJ (1994a) Exciton level structure and dynamics in the CP47 antenna complex of photosystem II. J Phys Chem 98:7717–7724CrossRefGoogle Scholar
  8. Chang H-C, Jankowiak R, Reddy NRS, Yocum CF, Picorel R, Seibert M, Small GJ (1994b) On the question of the chlorophyll a content of the photosystem II reaction center. J Phys Chem 98:7725–7735CrossRefGoogle Scholar
  9. Chauvet A, Jankowiak R, Kell A, Picorel R, Savikhin S (2015) Does the singlet minus triplet spectrum with major photobleaching band near 680–682 nm represent an intact reaction center of photosystem II? J Phys Chem B 119:448–455CrossRefPubMedGoogle Scholar
  10. Dang NC, Zazubovich V, Reppert M, Neupane B, Picorel R, Seibert M, Jankowiak R (2008) The CP43 proximal antenna complex of higher plant photosystem II revisited: modeling and hole burning study. I. J Phys Chem B 112:9921–9933CrossRefPubMedGoogle Scholar
  11. de Paula JC, Liefshitz A, Hinsley S, Lin W, Chopra V, Long K, Williams SA, Betts S, Yocum CF (1994) Structure-function relationships in the 47-kDa antenna protein and its complex with the photosystem II reaction center core: insights from picosecond fluorescence decay kinetics and resonance Raman spectroscopy. Biochemistry 33:1455–1466CrossRefPubMedGoogle Scholar
  12. den Hartog FTH, Dekker JP, van Grondelle R, Völker S (1998) Spectral distributions of “trap” pigments in the RC, CP47, and CP47–RC complexes of photosystem II at low temperature: a fluorescence line-narrowing and hole-burning study. J Phys Chem B 102:11007–11016CrossRefGoogle Scholar
  13. Feng X, Neupane B, Acharya K, Zazubovich V, Picorel R, Seibert M, Jankowiak R (2011) Spectroscopic study of the CP43′ complex and the PSI-CP43′ supercomplex of the cyanobacterium Synechocystis PCC 6803. J Phys Chem B 115:13339–13349CrossRefPubMedGoogle Scholar
  14. Groot M-L, Peterman, van Stokkum IHM, Dekker JP, van Grondelle R (1995) Triplet and fluorescing states of the CP47 antenna complex of Photosystem II studied as a function of temperature. Biophys J 68:281–290CrossRefPubMedCentralPubMedGoogle Scholar
  15. Groot M-L, Frese RN, de Weerd FL, Bromek K, Pettersson A, Peterman EJG, van Stokkum IHM, van Grondelle R, Dekker JP (1999) Spectroscopic properties of the CP43 core antenna protein of photosystem II. Biophys J 77:3328–3340CrossRefPubMedCentralPubMedGoogle Scholar
  16. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342CrossRefPubMedGoogle Scholar
  17. Hughes JL, Smith PJ, Pace RJ, Krausz E (2007) Low-energy absorption and luminescence of higher plant photosystem II core samples. J Lumin 122–123:284–287CrossRefGoogle Scholar
  18. Jankowiak R (2012) Probing electron-transfer times in photosynthetic reaction centers by hole-burning spectroscopy. J Phys Chem Lett 3:1684–1694CrossRefGoogle Scholar
  19. Jankowiak R, Hayes JM, Small GJ (2002) An excitonic pentamer model for the core Qy states of the isolated photosystem II reaction center. J Phys Chem B 106:8803–8814CrossRefGoogle Scholar
  20. Jankowiak R, Reppert M, Zazubovich V, Pieper J, Reinot T (2011) Site selective and single complex laser-based spectroscopies: a window on excited state electronic structure, excitation energy transfer, and electron–phonon coupling of selected photosynthetic complexes. Chem Rev 111:4546–4598CrossRefPubMedGoogle Scholar
  21. Komura M, Shibata Y, Itoh S (2006) A new fluorescence band F689 in photosystem II revealed by picosecond analysis at 4–77 K: function of two terminal energy sinks F689 and F695 in PS II. Biochim Biophys Acta 1757:1657–1668CrossRefPubMedGoogle Scholar
  22. 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 36:7498–7502CrossRefPubMedGoogle Scholar
  23. Krausz E, Hughes JL, Smith PJ, Pace RJ, Peterson Årsköld S (2005) Assignment of the low-temperature fluorescence in oxygen-evolving photosystem II. Photosynth Res 84:193–199CrossRefPubMedGoogle Scholar
  24. Kupitz C, Grotjohann I, Conrad CE, Roy-Chowhury S, Fromme R, Fromme P (2014a) Microcrystallization techniques for serial femtosecond crystallography using photosystem II from Thermosynechococcus elongatus as a model system. Philos Trans R Soc B 369:1471–2970CrossRefGoogle Scholar
  25. Kupitz C, Basu S, Grotjohann I, Fromme R, Zatsepin NA, Rendek KN, Hunter MS, Shoeman RL, White TA, Wang D et al (2014b) Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature 513:261–265CrossRefPubMedGoogle Scholar
  26. Kurreck J, Schödel R, Renger G (2000) Investigation of the plastoquinone pool size and fluorescence quenching in thylakoid membranes and photosystem II (PS II) membrane fragments. Photosynth Res 63:171–182CrossRefPubMedGoogle Scholar
  27. Kwa SLS, Tilly NT, Eijckelhoff C, van Grondelle R, Dekker JP (1994) Site-selection spectroscopy of the reaction center complex of photosystem II. 2. Identification of the fluorescence species at 4 K. J Phys Chem 98:7712–7716CrossRefGoogle Scholar
  28. Lewis KLM, Ogilvie JP (2012) Probing photosynthetic energy and charge transfer with two-dimensional electronic spectroscopy. J Phys Chem Lett 3:503–510CrossRefGoogle Scholar
  29. Lince MT, Vermaas W (1998) Association of His117 in the D2 protein of photosystem II with a chlorophyll that affects excitation-energy transfer efficiency to the reaction center. Eur J Biochem 256:595–602CrossRefPubMedGoogle Scholar
  30. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044CrossRefPubMedGoogle Scholar
  31. Masters V, Smith P, Krausz E, Pace R (2001) Stark shifts and exciton coupling in PSII ‘supercores’. J Lumin 94–95:267–270CrossRefGoogle Scholar
  32. Mathis P (ed) (1996) Photosynthesis: from light to biosphere. Proceedings of the Xth international photosynthesis congress. Springer, Dordrecht, The NetherlandsGoogle Scholar
  33. Morton J, Hall J, Smith P, Akita F, Koua FHM, Shen J-R, Krausz E (2014) Determination of the PS I content of PS II core preparations using selective emission: a new emission of PS II at 780 nm. Biochim Biophys Acta 1837:167–177CrossRefPubMedGoogle Scholar
  34. Müh F, Madjet ME-A, Renger T (2012) Structure-based simulation of linear optical spectra of the CP43 core antenna of photosystem II. Photosynth Res 111:87–101CrossRefPubMedGoogle Scholar
  35. Neupane B, Dang NC, Acharya K, Reppert M, Zazubovich V, Picorel R, Seibert M, Jankowiak R (2010) Insight into the electronic structure of the CP47 antenna protein complex of photosystem II: hole burning and fluorescence study. J Am Chem Soc 132:4214–4229CrossRefPubMedGoogle Scholar
  36. Peterman EJG, van Amerongen H, van Grondelle R, Dekker JP (1998) The nature of the excited state of the reaction center of photosystem II of green plants: a high-resolution fluorescence spectroscopy study. Proc Natl Acad Sci USA 95:6128–6133CrossRefPubMedCentralPubMedGoogle Scholar
  37. Prakash JSS, Baig MA, Bhagwat AS, Mohanty P (2003) Characterization of senescence-induced changes in light harvesting complex II and photosystem I complex of thylakoids of Cucumis sativus cotyledons: age induced association of LHCII with Photosystem I. J Plant Physiol 160:175–184CrossRefPubMedGoogle Scholar
  38. Raszewski G, Renger T (2008) Light harvesting in photosystem II core complexes is limited by the transfer to the trap: can the core complex turn into a photoprotective mode? J Am Chem Soc 130:4431–4446CrossRefPubMedGoogle Scholar
  39. Raszewski G, Saenger W, Renger T (2005) Theory of optical spectra of photosystem II reaction centers: location of the triplet state and the identity of the primary electron donor. Biophys J 88:986–998CrossRefPubMedCentralPubMedGoogle Scholar
  40. Renger T, Schlodder E (2010) Primary photophysical processes in photosystem II: bridging the gap between crystal structure and optical spectra. ChemPhysChem 11:1141–1153CrossRefPubMedGoogle Scholar
  41. Reppert M, Zazubovich V, Dang NC, Seibert M, Jankowiak R (2008) Low-energy chlorophyll states in the CP43 antenna protein complex: simulation of various optical spectra. II. J Phys Chem B 112:9934–9947CrossRefPubMedGoogle Scholar
  42. Reppert M, Acharya K, Neupane B, Jankowiak R (2010) Lowest electronic states of the CP47 antenna protein complex of photosystem II: simulation of optical spectra and revised structural assignments. J Phys Chem B 114:11884–11898CrossRefPubMedGoogle Scholar
  43. Riley K, Jankowiak R, Rätsep M, Small GJ, Zazubovich V (2004) Evidence for highly dispersive primary charge separation kinetics and gross heterogeneity in the isolated PS II reaction center of green plants. J Phys Chem B 108:10346–10356CrossRefGoogle Scholar
  44. Schweitzer RH, Melkozernov AN, Blankenship RE, Brudvig GW (1998) Time-resolved fluorescence measurements of photosystem II: the effect of quenching by oxidized chlorophyll Z. J Phys Chem B 102:8320–8326CrossRefGoogle Scholar
  45. Shibata Y, Nishi S, Kawakami K, Shen J-R, Renger T (2013) Photosystem II does not possess a simple excitation energy funnel: time-resolved fluorescence spectroscopy meets theory. J Am Chem Soc 135:6903–6914CrossRefPubMedCentralPubMedGoogle Scholar
  46. Sun R, Liu K, Dong L, Wu Y, Paulsen H, Yang C (2015) Direct energy transfer from the major antenna to the photosystem II core complexes in the absence of minor antennae in liposomes. Biochim Biophys Acta 1847:248–261CrossRefPubMedGoogle Scholar
  47. Tang D, Jankowiak R, Seibert M, Yocum CF, Small GJ (1990) Excited-state structure and energy-transfer dynamics of two different preparations of the reaction center of photosystem II: a hole-burning study. J Phys Chem 94:6519–6522CrossRefGoogle Scholar
  48. Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60CrossRefPubMedGoogle Scholar
  49. van der Weij–de Wit CD, Dekker JP, van Grondelle R, van Stokkum IHM (2011) Charge separation is virtually irreversible in photosystem II core complexes with oxidized primary quinone acceptor. J Phys Chem A 115:3947–3956CrossRefPubMedGoogle Scholar
  50. van Dorssen RJ, Plijter JJ, Dekker JP, den Ouden A, Amesz J, van Gorkom HJ (1987) Spectroscopic properties of chloroplast grana membranes and of the core of photosystem II. Biochim Biophys Acta 890:134–143CrossRefGoogle Scholar
  51. 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 1020:146–152CrossRefGoogle Scholar
  52. Wang J, Gosztola D, Ruffle SV, Hemann C, Seibert M, Wasielewski MR, Hille R, Gustafson TL, Sayre RT (2002) Functional asymmetry of photosystem II D1 and D2 peripheral chlorophyll mutants of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 99:4091–4096CrossRefPubMedCentralPubMedGoogle Scholar
  53. Wydrzynski T, Satoh K (eds) (2005) Photosystem II: the light-driven water:plastoquinone oxireductase. Springer, Dordrecht, The NetherlandsGoogle Scholar
  54. Zazubovich V, Jankowiak R, Riley K, Picorel R, Seibert M, Small GJ (2003) How fast is excitation energy transfer in the photosystem II reaction center in the low temperature limit? hole burning vs photon echo. J Phys Chem B 107:2862–2866CrossRefGoogle Scholar
  55. Zouni A, Jordan R, Schlodder E, Fromme P, Witt HT (2000) First photosystem II crystals capable of water oxidation. Biochim Biophys Acta 1457:103–105CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Jinhai Chen
    • 1
  • Adam Kell
    • 1
  • Khem Acharya
    • 1
  • Christopher Kupitz
    • 2
  • Petra Fromme
    • 2
  • Ryszard Jankowiak
    • 1
    • 3
  1. 1.Department of ChemistryKansas State UniversityManhattanUSA
  2. 2.Department of Chemistry and BiochemistryArizona State UniversityTempeUSA
  3. 3.Department of PhysicsKansas State UniversityManhattanUSA

Personalised recommendations