Photosynthetica 2018, 56(1):185-191 | DOI: 10.1007/s11099-018-0778-8

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

M. Yamada1, R. Nagao2, M. Iwai3, Y. Arai1, A. Makita1, H. Ohta4, T. Tomo4,*
1 Graduate School of Science, Tokyo University of Science, Tokyo, Japan
2 Research Institute for Interdisciplinary Science, Okayama University, Okayama, Japan
3 School of Life Science and Technology, Tokyo Institute of Technology, Kanagawa, Japan
4 Faculty of Science, Tokyo University of Science, Tokyo, Japan

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

Received: May 8, 2017; Accepted: August 16, 2017; Published: March 1, 2018  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Yamada, M., Nagao, R., Iwai, M., Arai, Y., Makita, A., Ohta, H., & Tomo, T. (2018). The PsbQ' protein affects the redox potential of the QA in photosystem II. Photosynthetica56(SPECIAL ISSUE), 185-191. doi: 10.1007/s11099-018-0778-8
Download citation

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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  8. Demeter S., Govindjee: Thermoluminescence in plants.-Physiol. Plantarum 75: 121-130, 1989. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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, 2008 Go to original source...
  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. Go to original source...
  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. Go to original source...
  15. Fagerlund R.D., Eaton-Rye J.J.: The lipoproteins of cyano bacterial photosystem II.-J. Photoch. Photobio. B 104: 191-203, 2011. Go to original source...
  16. Ferreira K.N., Iverson T.M., Maghlaoui K. et al.: Architecture of the photosynthetic oxygen-evolving center.-Science 303: 1831-1838, 2004. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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, 20
  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, 20 Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  36. Shevela D., Govindjee: Adventures with cyanobacteria: a personal perspective.-Front. Plant Sci. 2: 28, 2011. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  43. Vass I., Cser K.: Janus-faced charge recombinations in photosystem II photoinhibition.-Trends Plant Sci. 14: 200-205, 2009. Go to original source...
  44. Vass I., Govindjee: Thermoluminescence from the photosynthetic apparatus.-Photosynth. Res. 48: 117-126, 1996. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...