BACKGROUND: PsbO, the manganese-stabilising protein, is an indispensable extrinsic subunit of photosystem II. It plays a crucial role in the stabilisation of the water-splitting Mn4CaO5 cluster, which catalyses the oxidation of water to molecular oxygen by using light energy. PsbO was also demonstrated to have a weak GTPase activity that could be involved in regulation of D1 protein turnover. Our analysis of psbO sequences showed that many angiosperm species express two psbO paralogs, but the pairs of isoforms in one species were not orthologous to pairs of isoforms in distant species. RESULTS: Phylogenetic analysis of 91 psbO sequences from 49 land plant species revealed that psbO duplication occurred many times independently, generally at the roots of modern angiosperm families. In spite of this, the level of isoform divergence was similar in different species. Moreover, mapping of the differences on the protein tertiary structure showed that the isoforms in individual species differ from each other on similar positions, mostly on the luminally exposed end of the β-barrel structure. Comparison of these differences with the location of differences between PsbOs from diverse angiosperm families indicated various selection pressures in PsbO evolution and potential interaction surfaces on the PsbO structure. CONCLUSIONS: The analyses suggest that similar subfunctionalisation of PsbO isoforms occurred parallelly in various lineages. We speculate that the presence of two PsbO isoforms helps the plants to finely adjust the photosynthetic apparatus in response to variable conditions. This might be mediated by diverse GTPase activity, since the isoform differences predominate near the predicted GTP-binding site.

Department of Experimental Plant Biology Faculty of Science Charles University Prague Viničná 5 128 44 Praha 2 Czech Republic

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De Las RJ, Balsera M, Barber J. Evolution of oxygenic photosynthesis: genome-wide analysis of the OEC extrinsic proteins. Trends Plant Sci. 2004;9:18–25. PubMed

Burnap RL, Sherman LA. Deletion mutagenesis in Synechocystis sp. PCC6803 indicates that the manganese-stabilizing protein of photosystem II is not essential for oxygen evolution. Biochemistry. 1991;30:440–6. doi: 10.1021/bi00216a020. PubMed DOI

Mayfield SP, Bennoun P, Rochaix JD. Expression of the nuclear encoded OEE1 protein is required for oxygen evolution and stability of photosystem II particles in Chlamydomonas reinhardtii. EMBO J. 1987;6:313–8. PubMed PMC

Yi X, McChargue M, Laborde S, Frankel LK, Bricker TM. The Manganese-stabilizing Protein Is Required for Photosystem II Assembly/Stability and Photoautotrophy in Higher Plants. J Biol Chem. 2005;280:16170–4. doi: 10.1074/jbc.M501550200. PubMed DOI

Umena Y, Kawakami K, Shen J-R, Kamiya N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature. 2011;473:55–60. doi: 10.1038/nature09913. PubMed DOI

Nield J, Balsera M, Rivas JDL, Barber J. Three-dimensional Electron Cryo-microscopy Study of the Extrinsic Domains of the Oxygen-evolving Complex of Spinach ASSIGNMENT OF THE PsbO PROTEIN. J Biol Chem. 2002;277:15006–12. doi: 10.1074/jbc.M110549200. PubMed DOI

Caffarri S, Kouřil R, Kereïche S, Boekema EJ, Croce R. Functional architecture of higher plant photosystem II supercomplexes. EMBO J. 2009;28:3052–63. doi: 10.1038/emboj.2009.232. PubMed DOI PMC

Kouřil R, Oostergetel GT, Boekema EJ. Fine structure of granal thylakoid membrane organization using cryo electron tomography. Biochim Biophys Acta BBA - Bioenerg. 1807;2011:368–74. PubMed

De Las RJ, Barber J. Analysis of the Structure of the PsbO Protein and its Implications. Photosynth Res. 2004;81:329–43. doi: 10.1023/B:PRES.0000036889.44048.e4. PubMed DOI

Lundin B, Thuswaldner S, Shutova T, Eshaghi S, Samuelsson G, Barber J, et al. Subsequent events to GTP binding by the plant PsbO protein: Structural changes, GTP hydrolysis and dissociation from the photosystem II complex. Biochim Biophys Acta BBA - Bioenerg. 2007;1767:500–8. doi: 10.1016/j.bbabio.2006.10.009. PubMed DOI

Bricker TM, Roose JL, Fagerlund RD, Frankel LK, Eaton-Rye JJ. The extrinsic proteins of Photosystem II. Biochim Biophys Acta BBA - Bioenerg. 1817;2012:121–42. PubMed

Suorsa M, Aro E-M. Expression, assembly and auxiliary functions of photosystem II oxygen-evolving proteins in higher plants. Photosynth Res. 2007;93:89–100. doi: 10.1007/s11120-007-9154-4. PubMed DOI

Bricker TM, Frankel LK. Auxiliary functions of the PsbO, PsbP and PsbQ proteins of higher plant Photosystem II: A critical analysis. J Photochem Photobiol B. 2011;104:165–78. doi: 10.1016/j.jphotobiol.2011.01.025. PubMed DOI

Spetea C, Hundal T, Lundin B, Heddad M, Adamska I, Andersson B. Multiple evidence for nucleotide metabolism in the chloroplast thylakoid lumen. Proc Natl Acad Sci U S A. 2004;101:1409–14. doi: 10.1073/pnas.0308164100. PubMed DOI PMC

Seidler A. The extrinsic polypeptides of Photosystem II. Biochim Biophys Acta BBA - Bioenerg. 1996;1277:35–60. doi: 10.1016/S0005-2728(96)00102-8. PubMed DOI

The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000;408:796. doi: 10.1038/35048692. PubMed DOI

Murakami R, Ifuku K, Takabayashi A, Shikanai T, Endo T, Sato F. Characterization of an Arabidopsis thaliana mutant with impaired psbO, one of two genes encoding extrinsic 33-kDa proteins in photosystem II. FEBS Lett. 2002;523:138–42. doi: 10.1016/S0014-5793(02)02963-0. PubMed DOI

Murakami R, Ifuku K, Takabayashi A, Shikanai T, Endo T, Sato F. Functional dissection of two Arabidopsis PsbO proteins. FEBS J. 2005;272:2165–75. doi: 10.1111/j.1742-4658.2005.04636.x. PubMed DOI

Lundin B, Hansson M, Schoefs B, Vener AV, Spetea C. The Arabidopsis PsbO2 protein regulates dephosphorylation and turnover of the photosystem II reaction centre D1 protein. Plant J. 2007;49:528–39. doi: 10.1111/j.1365-313X.2006.02976.x. PubMed DOI

Dwyer SA, Chow WS, Yamori W, Evans JR, Kaines S, Badger MR, et al. Antisense reductions in the PsbO protein of photosystem II leads to decreased quantum yield but similar maximal photosynthetic rates. J Exp Bot. 2012;63:4781–95. doi: 10.1093/jxb/ers156. PubMed DOI PMC

Lundin B, Nurmi M, Rojas-Stuetz M, Aro E-M, Adamska I, Spetea C. Towards understanding the functional difference between the two PsbO isoforms in Arabidopsis thaliana—insights from phenotypic analyses of psbo knockout mutants. Photosynth Res. 2008;98:405–14. doi: 10.1007/s11120-008-9325-y. PubMed DOI

Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardeström P, Schröder W, et al. The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature. Plant J. 2006;47:720–34. doi: 10.1111/j.1365-313X.2006.02821.x. PubMed DOI

Allahverdiyeva Y, Mamedov F, Holmström M, Nurmi M, Lundin B, Styring S, et al. Comparison of the electron transport properties of the psbo1 and psbo2 mutants of Arabidopsis thaliana. Biochim Biophys Acta BBA - Bioenerg. 2009;1787:1230–7. doi: 10.1016/j.bbabio.2009.05.013. PubMed DOI

Bricker TM, Frankel LK. The psbo1 Mutant of Arabidopsis Cannot Efficiently Use Calcium in Support of Oxygen Evolution by Photosystem II. J Biol Chem. 2008;283:29022–7. doi: 10.1074/jbc.M805122200. PubMed DOI PMC

Fischer L, Lipavska H, Hausman J-F, Opatrny Z. Morphological and molecular characterization of a spontaneously tuberizing potato mutant: an insight into the regulatory mechanisms of tuber induction. BMC Plant Biol. 2008;8:117. doi: 10.1186/1471-2229-8-117. PubMed DOI PMC

Database of Expressed Sequence Tags, NCBI GenBank [http://www.ncbi.nlm.nih.gov/nucest]

Plant Genome Database [http://www.plantgdb.org/]

Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402. doi: 10.1093/nar/25.17.3389. PubMed DOI PMC

Altschul SF, Wootton JC, Gertz EM, Agarwala R, Morgulis A, Schäffer AA, et al. Protein database searches using compositionally adjusted substitution matrices. FEBS J. 2005;272:5101–9. doi: 10.1111/j.1742-4658.2005.04945.x. PubMed DOI PMC

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–9. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC

Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059–66. doi: 10.1093/nar/gkf436. PubMed DOI PMC

Miller MA, Pfeiffer W, Schwartz T. Gateway Computing Environments Workshop (GCE), 2010. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees; pp. 1–8.

Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688–90. doi: 10.1093/bioinformatics/btl446. PubMed DOI

Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012;40:D1178–86. doi: 10.1093/nar/gkr944. PubMed DOI PMC

The R Project for Statistical Computing [http://www.r-project.org/] PubMed

Charif D, Lobry JR: SeqinR 1.0-2: A Contributed Package to the R Project for Statistical Computing Devoted to Biological Sequences Retrieval and Analysis. In Structural Approaches to Sequence Evolution. Edited by Bastolla U, Porto M, Roman HE, Vendruscolo M. Springer Berlin Heidelberg; 2007:207–232. [Biological and Medical Physics, Biomedical Engineering]

Schwede T, Kopp J, Guex N, Peitsch MC. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 2003;31:3381–5. doi: 10.1093/nar/gkg520. PubMed DOI PMC

Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics. 2006;22:195–201. doi: 10.1093/bioinformatics/bti770. PubMed DOI

Guex N, Peitsch MC. SWISS-MODEL and the Swiss-Pdb Viewer: An environment for comparative protein modeling. Electrophoresis. 1997;18:2714–23. doi: 10.1002/elps.1150181505. PubMed DOI

POV-Ray - The Persistence of Vision Raytracer [http://www.povray.org/]

Flagel LE, Wendel JF. Gene duplication and evolutionary novelty in plants. New Phytol. 2009;183:557–64. doi: 10.1111/j.1469-8137.2009.02923.x. PubMed DOI

Fawcett JA, Maere S, de Peer YV. Plants with double genomes might have had a better chance to survive the Cretaceous–Tertiary extinction event. Proc Natl Acad Sci. 2009;106:5737–42. doi: 10.1073/pnas.0900906106. PubMed DOI PMC

Vanneste K, Baele G, Maere S, Peer YV de: Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Res 2014;24:1334–47. PubMed PMC

Hittinger CT, Carroll SB. Gene duplication and the adaptive evolution of a classic genetic switch. Nature. 2007;449:677–81. doi: 10.1038/nature06151. PubMed DOI

Liu H, Frankel LK, Bricker TM. Functional Analysis of Photosystem II in a PsbO-1-Deficient Mutant in Arabidopsis thaliana. Biochemistry. 2007;46:7607–13. doi: 10.1021/bi700107w. PubMed DOI

Ifuku K, Nakatsu T, Kato H, Sato F. Crystal structure of the PsbP protein of photosystem II from Nicotiana tabacum. EMBO Rep. 2004;5:362–7. doi: 10.1038/sj.embor.7400113. PubMed DOI PMC

Betts SD, Lydakis-Simantiris N, Ross JR, Yocum CF. The Carboxyl-Terminal Tripeptide of the Manganese-Stabilizing Protein Is Required for Quantitative Assembly into Photosystem II and for High Rates of Oxygen Evolution Activity†. Biochemistry. 1998;37:14230–6. doi: 10.1021/bi981305h. PubMed DOI

De Las RJ, Heredia P, Roman A. Oxygen-evolving extrinsic proteins (PsbO, P, Q, R): Bioinformatic and functional analysis. Biochim Biophys Acta BBA - Bioenerg. 2007;1767:575–82. doi: 10.1016/j.bbabio.2007.01.018. PubMed DOI

Dekker JP, Boekema EJ. Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta BBA - Bioenerg. 2005;1706:12–39. doi: 10.1016/j.bbabio.2004.09.009. PubMed DOI

Boekema EJ, van Breemen JFL, van Roon H, Dekker JP. Conformational Changes in Photosystem II Supercomplexes upon Removal of Extrinsic Subunits. Biochemistry. 2000;39:12907–15. doi: 10.1021/bi0009183. PubMed DOI

Williamson A. Structural and functional aspects of the MSP (PsbO) and study of its differences in thermophilic versus mesophilic organisms. Photosynth Res. 2008;98:365–89. doi: 10.1007/s11120-008-9353-7. PubMed DOI

Hong SK, Pawlikowski SA, Vander Meulen KA, Yocum CF. The oxidation state of the photosystem II manganese cluster influences the structure of manganese stabilizing protein. Biochim Biophys Acta BBA - Bioenerg. 2001;1504:262–74. doi: 10.1016/S0005-2728(00)00255-3. PubMed DOI

Aro E-M, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, et al. Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot. 2005;56:347–56. doi: 10.1093/jxb/eri041. PubMed DOI

Kouřil R, Wientjes E, Bultema JB, Croce R, Boekema EJ. High-light vs. low-light: Effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana. Biochim Biophys Acta BBA - Bioenerg. 1827;2013:411–9. PubMed

Kirchhoff H. Structural changes of the thylakoid membrane network induced by high light stress in plant chloroplasts. Philos Trans R Soc B Biol Sci. 2014;369:20130225. doi: 10.1098/rstb.2013.0225. PubMed DOI PMC

Herbstová M, Tietz S, Kinzel C, Turkina MV, Kirchhoff H. Architectural switch in plant photosynthetic membranes induced by light stress. Proc Natl Acad Sci. 2012;109:20130–5. doi: 10.1073/pnas.1214265109. PubMed DOI PMC

Huner NPA, Öquist G, Sarhan F. Energy balance and acclimation to light and cold. Trends Plant Sci. 1998;3:224–30. doi: 10.1016/S1360-1385(98)01248-5. DOI

Detailed insight into the dynamics of the initial phases of de novo RNA-directed DNA methylation in plant cells