Abstract
The PsbM (3.9 kDa) and PsbY (4.2 kDa) proteins are membrane-spanning, single-helix, subunits associated with the chlorophyll-binding CP47 pre-complex of photosystem II (PSII). Removal of PsbM resulted in accumulation of PSII pre-assembly complexes and impaired electron transfer between the primary (QA) and secondary (QB) plastoquinone electron acceptors of PSII indicating that the QB-binding site and bicarbonate binding to the non-heme iron were altered in this strain. Removal of PsbY alone had only a minor impact on PSII activity but deleting PsbY in the ΔPsbM background led to additional modification of the acceptor side resulting in ΔPsbM:ΔPsbY cells being susceptible to photodamage and this required protein synthesis for recovery. Addition of bicarbonate was able to compensate for the light-induced damage in ΔPsbM:ΔPsbY cells potentially re-occupying the modified bicarbonate-binding site in the ΔPsbM:ΔPsbY strain and complementation of ΔPsbM:ΔPsbY cells with the psbY gene restored the ΔPsbM phenotype.
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Abbreviations
- Chl:
-
chlorophyll
- CP43:
-
43 kDa chlorophyll-binding core antenna protein
- CP47:
-
47 kDa chlorophyll-binding core antenna protein
- DCBQ:
-
2,6-dichloro-1,4-benzoquinone
- DCMU:
-
3,4-dichloro-1,1-dimethyl urea
- DMBQ:
-
2,5-dimethyl-1,4- benzoquinone
- F:
-
fluorescence level
- Fm :
-
maximum fluorescence level
- Fo :
-
initial fluorescence level
- HEPES:
-
4-(2-hydroxyethyl)- 1-piperazineethanesulfonic acid
- LMW:
-
lte]ow molecular weight
- PCC:
-
Pasteur Culture Collection
- QA :
-
primary plastoquinone electron acceptor of PSII
- QB :
-
secondary plastoquinone electron acceptor of PS II
- RC47:
-
a PSII pre-assembly complex composed of the reaction center assembly module and the CP47 pre-complex assembly module
- S2:
-
the oxidation state of the oxygen-evolving complex following a single-turnover flash applied to dark-adapted cells
- TES:
-
2-[tris(hydroxymethyl)methyl]amino-1-ethanesulfonic acid
References
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.
Bentley F.K., Luo H., Dilbeck P. et al.: Effects of inactivating psbM and psbT on photodamage and assembly of Photosystem II in Synechocystis sp. PCC 6803.–Biochemistry 47: 11637–11646, 2008.
Boehm M., Yu J., Reisinger V. et al.: Subunit composition of CP43-less Photosystem II complexes of Synechocystis sp. PCC 6803: implications for the assembly and repair of photosystem II.–Phil. T. Roy. Soc. B 367: 3444–3454, 2012.
Boehm M., Romero E., Reisinger V. et al.: Investigating the early stages of Photosystem II assembly in Synechocystis sp. PCC 6803: isolation of CP47 and CP43 complexes.–J. Biol. Chem. 286: 14812–14819, 2011.
Bricker T.M., Roose J.L., Fagerlund R.D. et al.: The extrinsic proteins of Photosystem II.–Biochim. Biophys. Acta 1817: 121–142, 2012.
Brinkert K., Causmaecker S.D., Krieger-Liszkay A. et al.: Bicarbonate-induced redox tuning in photosystem II for regulation and protection.–P. Natl. Acad. Sci. USA 113: 12144–12149, 2016.
Bryksin A.V., Matsumura I.: Overlap extension PCR cloning: A simple and reliable way to create recombinant plasmids.–Biotechniques 48: 463–465, 2010.
Chu H.-A., Chiu Y.-F.: The roles of cytochrome b559 in assembly and photoprotection of photosystem II revealed by site-directed mutagenesis studies.–Front. Plant Sci. 6: 1261, 2016.
Crawford T.S., Eaton-Rye J.J., Summerfield T.C.: Mutation of Gly195 of the ChlH subunit of Mg-chelatase reduces chlorophyll and further disrupts PS II assembly in a Ycf48-deficient strain of Synechocystis sp. PCC 6803.–Front. Plant Sci. 7: 1060, 2016
Eaton-Rye J.J.: Construction of gene interruptions and gene deletions in the cyanobacterium Synechocystis sp. strain PCC 6803.–Methods Mol. Biol. 684: 295–312, 2011.
Eaton-Rye J.J., Govindjee: Electron transfer through the quinone acceptor complex of photosystem II in bicarbonate-depleted spinach thylakoid membranes as a function of actinic flash number and frequency.–BBA-Bioenergetics 935: 237–247, 1988a.
Eaton-Rye J.J., Govindjee: Electron transfer through the quinone accepter complex of Photosystem II after one or two actinic flashes in bicarbonate-depleted spinach thylakoid membranes.–BBA-Bioenergetics 935: 248–257, 1988b.
Jackson S.A., Hervey J.R.D., Dale A.J. et al.: Removal of both Ycf48 and Psb27 in Synechocystis sp. PCC 6803 disrupts Photosystem II assembly and alters QA− oxidation in the mature complex.–FEBS Lett. 588: 3751–3760, 2014.
Kawakami K., Iwai M., Ikeuchi M. et al.: Location of PsbY in oxygen-evolving photosystem II revealed by mutagenesis and X-ray crystallography.–FEBS Lett. 581: 4983–4987, 2007.
Kawakami K., Umena Y., Iwai M. et al.: Roles of PsbI and PsbM in Photosystem II dimer formation and stability studied by deletion mutagenesis and X-ray crystallography.–Biochim. Biophys. Acta 1807: 319–325, 2011.
Komenda J., Sobotka R., Nixon P.J.: Assembling and maintaining the Photosystem II complex in chloroplasts and cyanobacteria.–Curr. Opin. Plant Biol. 15: 245–251, 2012.
MacKinney G.: Absorption of light by chlorophyll solutions.–J. Biol. Chem. 140: 315–322, 1941.
Meetam M., Keren N., Ohad I. et al.: The PsbY protein is not essential for oxygenic photosynthesis in the cyanobacterium Synechocystis sp. PCC 6803.–Plant Physiol. 121: 1267–1272, 1999.
Morris J.N., Crawford T.S., Jeffs A. et al.: Whole genome resequencing of two “wild-type” strains of the model cyanobacterium Synechocystis sp. PCC 6803.–New Zeal. J. Bot. 52: 36–47, 2014.
Neufeld S., Zinchenko V., Stephan D.P. et al.: On the functional significance of the polypeptide PsbY for photosynthetic water oxidation in the cyanobacterium Synechocystis sp. strain PCC 6803.–Mol. Genet. Genomics 271: 458–467, 2004.
Nixon P.J., Komenda J., Barber J. et al.: Deletion of the PESTlike region of photosystem two modifies the QB-binding pocket but does not prevent rapid turnover of D1.–J. Biol. Chem. 270: 14919–14927, 1995.
Robinson H.H., Crofts A.R.: Kinetics of the oxidation-reduction reactions of the photosystem II quinone acceptor complex, and the pathway for deactivation.–FEBS Lett. 153: 221–226, 1983.
Robinson, H.H., Eaton-Rye, J.J., van Resen, J.J.S., Govindjee.: The effects of bicarbonate depletion and formate incubation on the kinetics of oxidation-reduction reactions of the Photosystem II quinone acceptor complex.–Z. Naturforsch. 39c: 382–385, 1984.
Sedoud A., Kastner L., Cox N. et al.: Effects of formate binding on the quinone-iron electron acceptor complex of Photosystem II.–Biochim. Biophys. Acta 1807: 216–226, 2011.
Shen J.-R.: The structure of Photosystem II, and the mechanism of water oxidation in photosynthesis.–Annu. Rev. Plant Biol. 66: 23–48, 2015.
Shi L.-X., Hall M., Funk C. et al.: Photosystem II, a growing complex: updates on newly discovered components and low molecular mass proteins.–Biochim. Biophys. Acta 1817: 13–25, 2012.
Shevela D., Eaton-Rye J.J., Shen J.-R., Govindjee: bicarbonate: A historical perspective.–Biochim. Biophys. Acta 1817: 1134–1151, 2012.
Stirbet A., Govindjee: On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient.–J. Photochem. Photobiol. B 104: 236–257, 2011.
Stirbet A., Riznichenko G.Y., Rubin A.B. et al.: Modeling chlorophyll a fluorescence transient: relation to photosynthesis.–Biochemistry-Moscow 79: 291–323, 2014.
Suga M., Akita F., Hirata K. et al.: Native structure of Photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses.–Nature 517: 99–103, 2015.
Suga M., Akita F., Sugahara M. et al.: Light-induced structural changes and the site of O = O bond formation in PSII caught by XFEL.–Nature 543:131–135, 2017.
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.
Uto S., Kawakami K., Umena Y. et al.: Mutational relationships between structural and functional changes in a PsbM-deletion mutants of Photosystem II.–Faraday Discuss. 198: 107–120, 2017.
Vass I., Kirilovsky D., Etienne A.: UV-B radiation-induced donor- and acceptor-side modifications of Photosystem II in the cyanobacterium Synechocystis sp. PCC 6803.–Biochemistry 38: 12786–12794, 1999.
Vinyard D.J., Brudvig G.W.: Progress towards a molecular mechanism of water oxidation in Photosystem II.–Annu. Rev. Phys. Chem. 68: 101–116, 2017.
von Sydow L.V., Schwenkert S., Meurer J. et al.: The PsbY protein of Arabidopsis photosystem II is important for the redox control of cytochrome b559.–Biochem. Biophys. Acta 1857: 1524–1533, 20
Wei X., Su X., Cao P. et al.: Spinach Photosystem II-LHCII supercomplex at 3.2 Å resolution.–Nature 534: 69–74, 2016.
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Acknowledgments: S.B. was supported by an Otago University PhD scholarship. We thank Matthew Prouse for construction of the ΔPsbM and ΔPsbY strains.
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Biswas, S., Eaton-Rye, J.J. PsbY is required for prevention of photodamage to photosystem II in a PsbM-lacking mutant of Synechocystis sp. PCC 6803. Photosynthetica 56, 200–209 (2018). https://doi.org/10.1007/s11099-018-0788-6
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DOI: https://doi.org/10.1007/s11099-018-0788-6