, Volume 49, Issue 4, pp 573–580 | Cite as

PsbO, PsbP, and PsbQ of photosystem II are encoded by gene families in Nicotiana benthamiana. Structure and functionality of their isoforms

  • M. L. Pérez-BuenoEmail author
  • M. Barón
  • I. García-Luque
Original Papers


The extrinsic proteins of photosystem II in plants (PsbO, PsbP and PsbQ) are known to be targets of stress. In previous work, differential regulation of hypothetical isoforms of these proteins was observed in Nicotiana benthamiana upon viral infection. Each of these proteins is encoded by a multigene family in this species: there are at least four genes encoding PsbO and PsbP and two encoding PsbQ. The results of structural and functional analyses suggest that PsbO and PsbP isoforms could show differences in activity, based on significant substitutions in their primary structure. Two psbQ sequences were isolated which encode identical mature proteins.

Additional key words

oxygen-evolving complex photosystem II PsbO PsbP PsbQ stress 



oxygen-evolving complex


isoelectric point


photosystem II


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The authors thank Dr. Maite Serra and Mario García for critical reading of the manuscript. MPB was recipient of a JAE-Doc contract funded by CSIC. This work was supported by grants BIO2004-04968-C02-02, and MCINN-FEDER/AGL2008-00450 to IGL and BIO2004-04968-C02-02, MEC-FEDER/BIO2007-67874-C02-02, MCINN-FEDER/AGL2008-00214 and CVI 03475 (Junta de Andalucía) to MBA.


  1. Arnold, K., Bordoli, L., Kopp, J., Schwede, T.: The SWISSMODEL workspace: a web-based environment for protein structure homology modelling. — Bioinformatics 22: 195–201, 2006.PubMedCrossRefGoogle Scholar
  2. Blouin, C., Butt, D., Roger, A.J.: Rapid evolution in conformational space: a study of loop regions in a ubiquitous GTP binding domain. — Protein Sci. 13: 608–616, 2004.PubMedCrossRefGoogle Scholar
  3. Bondarava, N., Beyer, P., Krieger-Liszkay, A.: Function of the 23 kDa extrinsic protein of Photosystem II as a manganese binding protein and its role in photoactivation. — Biochim. Biophys. Acta 1708: 63–70, 2005.PubMedCrossRefGoogle Scholar
  4. Bricker, T.M., Frankel, L.K.: Carboxylate groups on the manganese-stabilizing protein are required for efficient binding of the 24 kDa extrinsic protein to photosystem II. — Biochemistry 42: 2056–2061, 2003.PubMedCrossRefGoogle Scholar
  5. Chu, H.A., Nguyen, A.P., Debus, R.J.: Site-directed photosystem II mutants with perturbed oxygen-evolving properties. 2. Increased binding or photooxidation of manganese in the absence of the extrinsic 33-kDa polypeptide in vivo. — Biochemistry 33: 6150–6157, 1994.PubMedCrossRefGoogle Scholar
  6. de las Rivas, J., Barber, J.: Analysis of the structure of the PsbO protein and its implications. — Photosynth. Res. 81: 329–343, 2004.CrossRefGoogle Scholar
  7. de las Rivas, J., Roman, A.: Structure and evolution of the extrinsic proteins that stabilize the oxygen-evolving engine. — Photochem. Photobiol. Sci. 4: 1003–1010, 2005.CrossRefGoogle Scholar
  8. Eisenberg-Domovich, Y., Oelmuller, R., Herrmann, R.G., Ohad, I.: Role of the RCII-D1 protein in the reversible association of the oxygen-evolving complex proteins with the lumenal side of photosystem II. — J. Biol. Chem. 270: 30181–30186, 1995.PubMedCrossRefGoogle Scholar
  9. Emanuelsson, O., Nielsen, H., Brunak, S., Von Heijne, G.: Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. — J. Mol. Biol. 300: 1005–1016, 2000.PubMedCrossRefGoogle Scholar
  10. Enami, I., Okumura, A., Nagao, R., Suzuki, T., Iwai, M., Shen, J.R.: Structures and functions of the extrinsic proteins of photosystem II from different species. — Photosynth. Res. 98: 349–363, 2008.PubMedCrossRefGoogle Scholar
  11. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S.E., Wilkins, M.R., Appel, R.D., Bairoch, A.: Protein Identification and Analysis Tools on the ExPASy Server. — In: (ed.): The Proteomics Protocols Handbook. Pp. 571–607. 2005.Google Scholar
  12. Gouet, P., Courcelle, E., Stuart, D.I., Metoz, F.: ESPript: multiple sequence alignments in PostScript. — Bioinformatics 15: 305–308, 1999.PubMedCrossRefGoogle Scholar
  13. Ido, K., Ifuku, K., Yamamoto, Y., Ishihara, S., Murakami, A., Takabe, K., Miyake, C., Sato, F.: Knockdown of the PsbP protein does not prevent assembly of the dimeric PSII core complex but impairs accumulation of photosystem II supercomplexes in tobacco. — Biochim. Biophys. Acta 1787: 873–881, 2009.PubMedCrossRefGoogle Scholar
  14. Ifuku, K., Nakatsu, T., Kato, H. Sato, F.: Crystal structure of the PsbP protein of photosystem II from Nicotiana tabacum — EMBO Rep. 5: 362–367, 2004.PubMedCrossRefGoogle Scholar
  15. Ifuku, K., Nakatsu, T., Shimamoto, R., Yamamoto, Y., Ishihara, S., Kato, H., Sato, F.: Structure and function of the PsbP protein of Photosystem II from higher plants. — Photosynth. Res. 84: 251–255, 2005.PubMedCrossRefGoogle Scholar
  16. Ifuku, K., Sato, F.: Importance of the N-terminal sequence of the extrinsic 23 kDa polypeptide in Photosystem II in ion retention in oxygen evolution. — Biochim. Biophys. Acta 1546: 196–204, 2001.PubMedCrossRefGoogle Scholar
  17. Ifuku, K., Sato, F.: A truncated mutant of the extrinsic 23-kDa protein that absolutely requires the extrinsic 17-kDa protein for Ca2+ retention in photosystem II. — Plant Cell Physiol. 43: 1244–1249, 2002.PubMedCrossRefGoogle Scholar
  18. Ishihara, S., Yamamoto, Y., Ifuku, K., Sato, F.: Functional analysis of four members of the PsbP family in photosystem II in Nicotiana tabacum using differential RNA interference. — Plant Cell Physiol. 46: 1885–1893, 2005.PubMedCrossRefGoogle Scholar
  19. Komenda, J., Knoppová, J., Krynická, V., Nixon, P.J., Tichý, M.: Role of FtsH2 in the repair of Photosystem II in mutants of the cyanobacterium Synechocystis PCC 6803 with impaired assembly or stability of the CaMn4 cluster. — Biochim. Biophys. Acta 1797: 566–575, 2010.PubMedCrossRefGoogle Scholar
  20. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G.: Clustal W and Clustal X version 2.0. — Bioinformatics 23: 2947–2948, 2007.PubMedCrossRefGoogle Scholar
  21. Logemann, J., Schell, J., Willmitzer, L.: Improved method for the isolation of RNA from plant tissues. — Anal. Biochem. 163: 16–20, 1987.PubMedCrossRefGoogle Scholar
  22. Loll, B., Kern, J., Saenger, W., Zouni, A., Biesiadka, J.: Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. — Nature 438: 1040–1044, 2005.PubMedCrossRefGoogle Scholar
  23. Lundin, B., Hansson, M., Schoefs, B., Vener, A.V., Spetea, C.: The Arabidopsis PsbO2 protein regulates dephosphorylation and turnover of the photosystem II reaction centre D1 protein. — Plant J. 49: 528–539, 2007a.PubMedCrossRefGoogle Scholar
  24. Lundin, B., Thuswaldner, S., Shutova, T., Eshaghi, S., Samuelsson, G., Barber, J., Andersson, B., Spetea, C.: Subsequent events to GTP binding by the plant PsbO protein: Structural changes, GTP hydrolysis and dissociation from the photosystem II complex. — Biochim. Biophys. Acta 1767: 500–508, 2007b.PubMedCrossRefGoogle Scholar
  25. Murakami, R., Ifuku, K., Takabayashi, A., Shikanai, T., Endo, T., Sato, F.: Functional dissection of two Arabidopsis PsbO proteins: PsbO1 and PsbO2. — FEBS J. 272: 2165–2175, 2005.PubMedCrossRefGoogle Scholar
  26. Nield, J., Barber, J.: Refinement of the structural model for the Photosystem II supercomplex of higher plants. — Biochim. Biophys. Acta 1757: 353–361, 2006.PubMedCrossRefGoogle Scholar
  27. Peltier, J.B., Friso, G., Kalume, D.E., Roepstorff, P., Adamaska, I., van Wick, K.J.: Proteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. — Plant Cell 12: 319–341, 2000.PubMedCrossRefGoogle Scholar
  28. Pérez-Bueno, M.L., Rahoutei, J., Sajnani, C., García-Luque, I., Barón, M.: Proteomic analysis of the oxygen-evolving complex of photosystem II under biotec stress: Studies on Nicotiana benthamiana infected with tobamoviruses. — Proteomics 4: 418–425, 2004.PubMedCrossRefGoogle Scholar
  29. Popelkova, H., Commet, A., Kuntzleman, T., Yocum, C.F.: Inorganic cofactor stabilization and retention: the unique functions of the two PsbO subunits of eukaryotic photosystem II. — Biochemistry 47: 12593–12600, 2008.PubMedCrossRefGoogle Scholar
  30. Rahoutei, J., Garcia-Luque, I., Baron, M.: Inhibition of photosynthesis by viral infection: Effect on PSII structure and function. — Physiol. Plant. 110: 286–292, 2000.CrossRefGoogle Scholar
  31. Seidler, A.: The extrinsic polypeptides of Photosystem II. — Biochim. Biophys. Acta 1277: 35–60, 1996.PubMedCrossRefGoogle Scholar
  32. Suorsa, M., Aro, E.M.: Expression, assembly and auxiliary functions of photosystem II oxygen-evolving proteins in higher plants. — Photosynth. Res. 93: 89–100, 2007.PubMedCrossRefGoogle Scholar
  33. Takahashi, H., Ehara, Y., Hirano, H.: A protein in the oxygenevolving complex in the chloroplast is associated with symptom expression on tobacco leaves infected with cucumber mosaic virus strain Y. — Plant Mol. Biol. 16: 689–698, 1991.PubMedCrossRefGoogle Scholar
  34. Tohri, A., Dohmae, N., Suzuki, T., Ohta, H., Inoue, Y., Enami, I.: Identification of domains on the extrinsic 23 kDa protein possibly involved in electrostatic interaction with the extrinsic 33 kDa protein in spinach photosystem II. — Eur. J. Biochem. 271: 962–971, 2004.PubMedCrossRefGoogle Scholar
  35. Yamamoto, Y., Ishikawa, Y., Nakatani, E., Yamada, M., Zhang, H., Wydrzynski, T.: Role of an extrinsic 33 kilodalton protein of photosystem II in the turnover of the reaction centerbinding protein D1 during photoinhibition. — Biochemistry 37: 1565–1574, 1998.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • M. L. Pérez-Bueno
    • 1
    • 2
    Email author
  • M. Barón
    • 1
  • I. García-Luque
    • 1
  1. 1.Departamento de Bioquímica y Biología Molecular y Celular de Plantas. Estación Experimental del ZaidínCSICGranadaSpain
  2. 2.Departamento de Biología Medioambiental, Centro de Investigaciones BiológicasCSICMadridSpain

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