Photosynthetica 2018, 56(1):200-209 | DOI: 10.1007/s11099-018-0788-6

PsbY is required for prevention of photodamage to photosystem II in a PsbM-lacking mutant of Synechocystis sp. PCC 6803

S. Biswas1, J. J. Eaton-Rye1,*
1 Department of Biochemistry, University of Otago, Dunedin, New Zealand

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.

Additional key words: assembly; bicarbonate; chlorophyll fluorescence; cytochrome b559; photoinhibition; repair

Received: October 3, 2017; Accepted: December 19, 2017; Published: March 1, 2018  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Biswas, S., & Eaton-Rye, J.J. (2018). PsbY is required for prevention of photodamage to photosystem II in a PsbM-lacking mutant of Synechocystis sp. PCC 6803. Photosynthetica56(SPECIAL ISSUE), 200-209. doi: 10.1007/s11099-018-0788-6
Download citation

Supplementary files

Download filephs-201801-0018_S1.pdf

File size: 329.81 kB

Download filephs-201801-0018_S2.pdf

File size: 199.76 kB

Download filephs-201801-0018_S3.pdf

File size: 164.19 kB

Download filephs-201801-0018_S4.pdf

File size: 254.06 kB

Download filephs-201801-0018_S5.pdf

File size: 204.86 kB

Download filephs-201801-0018_S6.pdf

File size: 188.69 kB

Download filephs-201801-0018_S7.pdf

File size: 79.31 kB

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. 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. Go to original source...
  3. 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. Go to original source...
  4. 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. 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. 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. Go to original source...
  7. Bryksin A.V., Matsumura I.: Overlap extension PCR cloning: A simple and reliable way to create recombinant plasmids.-Biotechniques 48: 463-465, 2010. Go to original source...
  8. 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. Go to original source...
  9. 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 Go to original source...
  10. 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. Go to original source...
  11. 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. Go to original source...
  12. 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. Go to original source...
  13. 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. Go to original source...
  14. 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. Go to original source...
  15. 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. Go to original source...
  16. 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. Go to original source...
  17. MacKinney G.: Absorption of light by chlorophyll solutions.-J. Biol. Chem. 140: 315-322, 1941. Go to original source...
  18. 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. Go to original source...
  19. 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. Go to original source...
  20. 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. Go to original source...
  21. 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. Go to original source...
  22. 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. Go to original source...
  23. 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. Go to original source...
  24. 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. Go to original source...
  25. Shen J.-R.: The structure of Photosystem II, and the mechanism of water oxidation in photosynthesis.-Annu. Rev. Plant Biol. 66: 23-48, 2015. Go to original source...
  26. 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. Go to original source...
  27. Shevela D., Eaton-Rye J.J., Shen J.-R., Govindjee: bicarbonate: A historical perspective.-Biochim. Biophys. Acta 1817: 1134-1151, 2012. Go to original source...
  28. 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. Go to original source...
  29. Stirbet A., Riznichenko G.Y., Rubin A.B. et al.: Modeling chlorophyll a fluorescence transient: relation to photosynthesis.-Biochemistry-Moscow 79: 291-323, 2014. Go to original source...
  30. 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. Go to original source...
  31. 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. Go to original source...
  32. 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...
  33. 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. Go to original source...
  34. 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. Go to original source...
  35. 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. Go to original source...
  36. 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 Go to original source...
  37. Wei X., Su X., Cao P. et al.: Spinach Photosystem II-LHCII supercomplex at 3.2 Å resolution.-Nature 534: 69-74, 2016. Go to original source...