Photosynthetica

, Volume 56, Issue 1, pp 185–191 | Cite as

The PsbQ′ protein affects the redox potential of the QA in photosystem II

  • M. Yamada
  • R. Nagao
  • M. Iwai
  • Y. Arai
  • A. Makita
  • H. Ohta
  • T. Tomo
Article
  • 22 Downloads

Abstract

Red alga contains four extrinsic proteins in photosystem II (PSII), which are PsbO, PsbV, PsbU, and PsbQ′. Except for the PsbQ′, the composition is the same in cyanobacterial PSII. Reconstitution analysis of cyanobacterial PSII has shown that oxygen-evolving activity does not depend on the presence of PsbQ′. Recently, the structure of red algal PSII was elucidated. However, the role of PsbQ′ remains unknown. In this study, the function of the acceptor side of PSII was analyzed in PsbQ′-reconstituted PSII by redox titration of QA and thermoluminescence. The redox potential of QA was positively shifted when PsbQ′ was attached to the PSII. The positive shift of QA is thought to cause a decrease in the amount of triplet chlorophyll in PSII. On the basis of these results, we propose that PsbQ′ has a photoprotective function when irradiated with strong light.

Additional key words

diversity evolution photoinhibition photosynthesis 

Abbreviation

Chl

chlorophyll

CP43

chlorophyll protein 43 kDa

CP47

chlorophyll protein 47 kDa

DCMU

3-(3,4-dichlorophenyl)-1,1-dimethylurea

IPTG

isopropyl β-D-1-thiogalactopyranoside

Ni-NTA

nickel-nitrilotriacetic acid

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ago H., Adachi H., Umena Y. et al.: Novel features of eukaryotic photosystem II revealed by its crystal structure analysis from a red alga.–J. Biol. Chem. 291: 5676–5687, 2016.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Allakhverdiev S.I., Tsuchiya T., Watabe K. et al.: Redox potentials of primary electron acceptor quinone molecule (QA)- and conserved energetics of photosystem II in cyanobacteria with chlorophyll a and chlorophyll d.–P. Natl. Acad. Sci. USA 108: 8054–8058, 2011.CrossRefGoogle Scholar
  3. Balsera M., Arellano J.B., Revuelta J.L. et al.: The 1.49 A resolution crystal structure of PsbQ from photosystem II of Spinacia oleracea reveals a PPII structure in the N-terminal region.–J. Mol. Biol. 350: 1051–1060, 2005.CrossRefPubMedGoogle Scholar
  4. Björn L.O.: The evolution of photosynthesis and its environmental impact.–In: Björn L.O. (ed.): Photobiology. Pp. 207–230. Springer, New York 2015.Google Scholar
  5. Bricker T.M., Roose J.L., Fagerlund R.D. et al.: The extrinsic proteins of Photosystem II.–Biochim. Biophys. Acta 1817: 121–142, 2012.CrossRefPubMedGoogle Scholar
  6. Calderone V., Trabucco M, Vujičić A. et al.: Crystal structure of the PsbQ protein of photosystem II from higher plants.–EMBO Rep. 4: 900–905, 2003.CrossRefPubMedPubMedCentralGoogle Scholar
  7. De Las Rivas J., Balsera M., Barber J.: Evolution of oxygenic photosynthesis: genome-wide analysis of the OEC extrinsic proteins.–Trends Plant Sci. 9: 18–25, 2004.CrossRefPubMedGoogle Scholar
  8. Demeter S., Govindjee: Thermoluminescence in plants.–Physiol. Plantarum 75: 121–130, 1989.CrossRefGoogle Scholar
  9. Eaton-Rye J.J.: Requirements for different combinations of the extrinsic proteins in specific cyanobacterial photosystem II mutants.–Photosynth. Res. 84: 275–281, 2005.CrossRefPubMedGoogle Scholar
  10. Enami I., Kikuchi S., Fukuda T. et al.: Binding and functional properties of four extrinsic proteins of photosystem II from a red alga, Cyanidium caldarium, as studied by release-reconstitution experiments.–Biochemistry 37: 2787–2793, 1998.CrossRefPubMedGoogle Scholar
  11. Enami I., Suzuki T., Tada O. et al.: Distribution of the extrinsic proteins as a potential marker for the evolution of photosynthetic oxygen-evolving photosystem II.–FEBS J. 272: 5020–5030, 2005.CrossRefPubMedGoogle Scholar
  12. Enami I., Okumura A., Nagao R. et al.: Structure and functions of the extrinsic proteins of photosystem II from different species.–Photosynth. Res. 98: 349–363, 2008CrossRefPubMedGoogle Scholar
  13. Enami I., Tohri A., Kamo M. et al.: Identification of domains on the 43 kDa chlorophyll-carrying protein (CP43) that are shielded from tryptic attack by binding of the extrinsic 33 kDa protein with photosystem II complex.–Biochim. Biophys. Acta 1320: 17–26, 1997.CrossRefPubMedGoogle Scholar
  14. Endo K., Mizusawa N., Shen J.-R. et al.: Site-directed mutagenesis of amino acid residues of D1 protein interacting with phosphatidylglycerol affects the function of plastoquinone QB in photosystem II.–Photosynth. Res. 126: 385–397, 2015.CrossRefPubMedGoogle Scholar
  15. Fagerlund R.D., Eaton-Rye J.J.: The lipoproteins of cyano bacterial photosystem II.–J. Photoch. Photobio. B 104: 191–203, 2011.CrossRefGoogle Scholar
  16. Ferreira K.N., Iverson T.M., Maghlaoui K. et al.: Architecture of the photosynthetic oxygen-evolving center.–Science 303: 1831–1838, 2004.CrossRefPubMedGoogle Scholar
  17. Ghanotakis D.F., Topper J.N., Babcock G.T. et al.: Watersoluble 17 and 23 kDa polypeptides restore oxygen evolution activity by creating a high-affinity binding site for Ca2+ on the oxidizing side of photosystem II.–FEBS Lett. 170: 169–173, 1984.CrossRefGoogle Scholar
  18. Ido K., Gross C.M., Guerrero F. et al.: High and low potential forms of the QA quinone electron acceptor in Photosystem II of Thermosynechococcus elongatus and spinach.–J. Photoch. Photobio. B 104: 154–157, 2011.CrossRefGoogle Scholar
  19. Ifuku K., Ido K., Sato F.: Molecular functions of PsbP and PsbQ proteins in the photosystem II supercomplex.–J. Photoch. Photobio. B 104: 158–164, 2011.CrossRefGoogle Scholar
  20. Iwai M., Katoh H., Katayama M. et al.: PSII-Tc protein plays an important role in dimerization of photosystem II.–Plant Cell Physiol. 45: 1809–1816, 2004.CrossRefPubMedGoogle Scholar
  21. Jackson S.A., Fagerlund R.D., Wilbanks S.M. et al.: Crystal structure of PsbQ from Synechocystis sp. PCC 6803 at 1.8 Å: implications for binding and function in cyanobacterial photosystem II.–Biochemistry 49: 2765–2767, 2010.CrossRefPubMedGoogle Scholar
  22. Johnson G.N., Rutherford A.W., Krieger A.: A change in the midpoint potential of the quinone QA in photosystem II associated with photoactivation of oxygen evolution.–BBABioenergetics 1229: 202–207, 1995.CrossRefGoogle Scholar
  23. Kato Y., Ishii R., Noguchi T.: Comparative analysis of the interaction of the primary quinone QA in intact and Mndepleted photosystem II membranes using light-induced ATRFTIR spectroscopy.–Biochemistry 55: 6355–6358, 2016.CrossRefPubMedGoogle Scholar
  24. Kato Y., Nagao R., Noguchi T.: acceptor QB in photosystem II reveals the mechanism of electron transfer regulation.–P. Natl. Acad. Sci. USA 113: 620–625, 2016.CrossRefGoogle Scholar
  25. Krieger A., Rutherford A.W., Johnson G.N.: On the determination of redox midpoint potential of the primary quinone electron acceptor, QA, in photosystem II.–BBA-Bioenergetics 1229: 193–201, 1995.CrossRefGoogle Scholar
  26. Loll B., Kern J., Saenger W. et al.: Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II.–Nature 438: 1040–1044, 2005.CrossRefPubMedGoogle Scholar
  27. Miyao M., Murata N.: The mode of binding of three extrinsic proteins of 33 kDa, 23 kDa and 18 kDa in the photosystem II complex of spinach.–BBA-Bioenergetics 977: 315–321, 1989.CrossRefGoogle Scholar
  28. Nagao R., Suga M., Niikura A. et al.: Crystal structure of Psb31, a novel extrinsic protein of photosystem II from a marine centric diatom and implications for its binding and function.–Biochemistry 52: 6646–6652, 2013.CrossRefPubMedGoogle Scholar
  29. Nagao R., Tomo T., Narikawa R. et al.: Conversion of photosystem II dimer to monomers during photoinhibition is tightly coupled with decrease in oxygen-evolving activity in the diatom Chaetoceros gracilis.–Photosynth. Res. 130: 83–91, 20CrossRefPubMedGoogle Scholar
  30. Nagao R., Tomo T., Noguchi E. et al.: Purification and charac terization of a stable oxygen-evolving Photosystem II complex from a marine centric diatom, Chaetoceros gracilis.–BBABioenergetics 1797: 160–166, 20CrossRefGoogle Scholar
  31. Noguchi T., Katoh M., Inoue Y.: A new system for detection of thermoluminescence and delayed luminescence from photosynthetic apparatus with precise temperature control.–J. Spectrosc. 16: 89–94, 2002.CrossRefGoogle Scholar
  32. Ohta H., Suzuki T., Ueno M. et al.: Extrinsic proteins of photosystem II: An intermediate member of the PsbQ protein family in red algal PS II.–Eur. J. Biochem. 270: 4156–4163, 2003.CrossRefPubMedGoogle Scholar
  33. Porra R., Thompson W., Kriedemann P.: Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.–BBABioenergetics 975: 384–394, 1989.CrossRefGoogle Scholar
  34. Rutherford A.W., Osyczka A., Rappaport F.: Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O2.–FEBS Lett. 586: 603–616, 2012.CrossRefPubMedGoogle Scholar
  35. Shen J.-R., Inoue Y.: Binding and functional properties of two new extrinsic Components, Cytochrome c-550 and a 12-kDa protein, in cyanobacterial photosystem II.–Biochemistry 32: 1825–1832, 1993.CrossRefPubMedGoogle Scholar
  36. Shevela D., Govindjee: Adventures with cyanobacteria: a personal perspective.–Front. Plant Sci. 2: 28, 2011.PubMedPubMedCentralGoogle Scholar
  37. Shibamoto T., Kato Y., Nagao R. et al.: Species-dependence of the redox potential of the primary quinone electron acceptor QA in photosystem II verified by spectroelectrochemistry.–FEBS Lett. 584: 1526–1530, 2010.CrossRefPubMedGoogle Scholar
  38. Shibamoto T., Kato Y., Sugiura M. et al.: Redox potential of the primary plastoquinone electron acceptor QA in photosystem II from Thermosynechococcus elongatus determined by spectroelectrochemistry.–Biochemistry 48: 10682–10684, 2009.CrossRefPubMedGoogle Scholar
  39. Suga M., Akita F., Hirata K. et al.: Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond Xray pulses.–Nature 517: 99–103, 2015.CrossRefPubMedGoogle Scholar
  40. Tomo T., Kato Y., Suzuki T. et al.: Characterization of highly purified photosystem I complexes from the chlorophyll ddominated cyanobacterium Acaryochloris marina MBIC 11017.–J. Biol. Chem. 283: 18198–18209, 2008.CrossRefPubMedGoogle Scholar
  41. Umena Y., Kawakami K., Shen J.-R. et al.: Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å.–Nature 473: 55–60, 2011.CrossRefPubMedGoogle Scholar
  42. Uno C., Nagao R., Suzuki H. et al.: Structural coupling of extrinsic proteins with the oxygen-evolving center in red algal photosystem II as revealed by light-induced FTIR difference spectroscopy.–Biochemistry 52: 5705–5707, 2013.CrossRefPubMedGoogle Scholar
  43. Vass I., Cser K.: Janus-faced charge recombinations in photosystem II photoinhibition.–Trends Plant Sci. 14: 200–205, 2009.CrossRefPubMedGoogle Scholar
  44. Vass I., Govindjee: Thermoluminescence from the photosynthetic apparatus.–Photosynth. Res. 48: 117–126, 1996.CrossRefPubMedGoogle Scholar
  45. Vass I., Kirilovsky D., Etienne A.-L.: UV-B radiation-induced donor- and acceptor-side modifications of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803.–Biochemistry 38: 12786–12794, 1999.CrossRefPubMedGoogle Scholar
  46. Vass I., Horváth G., Herczeg T. et al.: Photosynthetic energy conservation investigated by thermoluminescence. Activation energies and half-lives of thermoluminescence bands of chloroplasts determined by mathematical resolution of glow curves.–Biochim. Biophys. Acta 634: 140–152, 1981.CrossRefPubMedGoogle Scholar
  47. Wei X., Su X., Cao P. et al.: Structure of spinach photosystem II–LHCII supercomplex at 3.2 Å resolution.–Nature 534: 69–74, 2016.CrossRefPubMedGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  • M. Yamada
    • 1
  • R. Nagao
    • 2
  • M. Iwai
    • 3
  • Y. Arai
    • 1
  • A. Makita
    • 1
  • H. Ohta
    • 4
  • T. Tomo
    • 4
  1. 1.Graduate School of ScienceTokyo University of ScienceTokyoJapan
  2. 2.Research Institute for Interdisciplinary ScienceOkayama UniversityOkayamaJapan
  3. 3.School of Life Science and TechnologyTokyo Institute of TechnologyKanagawaJapan
  4. 4.Faculty of ScienceTokyo University of ScienceTokyoJapan

Personalised recommendations