Skip to main content
Springer Nature Link
Log in

The PsbZ subunit of Photosystem II in Synechocystis sp. PCC 6803 modulates electron flow through the photosynthetic electron transfer chain

  • Research Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The psbZ gene of Synechocystis sp. PCC 6803 encodes the ∼6.6 kDa photosystem II (PSII) subunit. We here report biophysical, biochemical and in vivo characterization of Synechocystis sp. PCC 6803 mutants lacking psbZ. We show that these mutants are able to perform wild-type levels of light-harvesting, energy transfer, PSII oxygen evolution, state transitions and non-photochemical quenching (NPQ) under standard growth conditions. The mutants grow photoautotrophically; however, their growth rate is clearly retarded under low-light conditions and they are not capable of photomixotrophic growth. Further differences exist in the electron transfer properties between the mutants and wild type. In the absence of PsbZ, electron flow potentially increased through photosystem I (PSI) without a change in the maximum electron transfer capacity of PSII. Further, rereduction of P700+ is much faster, suggesting faster cyclic electron flow around PSI. This implies a role for PsbZ in the regulation of electron transfer, with implication for photoprotection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

CP1:

Major chlorophyll a-protein of PSI

cyt b6f:

Cytochrome b6f

DCBQ:

2,6-Dichloro-p-benzoquinone

EPR:

Electron paramagnetic resonance

LHC:

Light-harvesting complex

NPQ:

Non-photochemical quenching

orf :

Open reading frame

P700:

Reaction centre chlorophyll of photosystem I

P700+ :

Oxidized P700

References

  • Anderson JM, Chow WS, Park Y-I (1995) The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46:129–139

    Article  CAS  Google Scholar 

  • Arteni AA, Nowaczyk M, Lax J, Kouril R, Rogner M, Boekema EJ (2005) Single particle electron microscopy in combination with mass spectrometry to investigate novel complexes of membrane proteins. J Struct Biol 149:325–331

    Article  CAS  PubMed  Google Scholar 

  • Baena Gonzalez E, Gray JC, Tyystjärvi E, Aro E-M, Mäenpää P (2001) Abnormal regulation of photosynthetic electron transport in a chloroplast ycf9 inactivation mutant. J Biol Chem 276:20795–20802

    Article  CAS  PubMed  Google Scholar 

  • Bendall DS, Manasse RS (1995) Cyclic photophosphorylation and electron transport. Biochim Biophys Acta 1229:23–38

    Article  Google Scholar 

  • Bishop CL, Purton S, Nugent JHA (2003) Molecular analysis of the Chlamydomonas nuclear gene encoding PsbW and demonstration that PsbW is a subunit of photosystem II, but not photosystem I. Plant Mol Biol 52:285–289

    Article  CAS  PubMed  Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24

    Article  CAS  Google Scholar 

  • Douglas SE, Penny SL (1999) The plastid genome of the cryptophyte alga, Guillardia theta: complete sequence and conserved synteny groups confirm its common ancestry with red algae. J Mol Evol 48:236–244

    Article  CAS  PubMed  Google Scholar 

  • Ferreira KN, Iverson TM, Magjlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

    Article  CAS  PubMed  Google Scholar 

  • Finazzi G, Furia A, Barbagallo RP, Forti G (1999) State transitions, cyclic and linear electron transport and photophosphorylation in Chlamydomonas reinhardtii. Biochim Biophys Acta 1413:117–129

    Article  CAS  PubMed  Google Scholar 

  • Hihara Y, Sonoike K (2001) Regulation, inhibition and protection of photosystem I. In: Anderson B, Aro EM (eds) Advances in photosynthesis XI, regulation of photosynthesis. Kluwer Academic, The Netherlands, pp 507–531

    Google Scholar 

  • Horton P (1996) Nonphotochemical quenching of chlorophyll fluorescence. In: Jennings RC, Zucchelli G, Ghetti F, Colombetti G (eds) Light as energy source and information carrier in plant physiology. Plenum Press, New York, pp 99–112

    Google Scholar 

  • Hupfer H, Swiatek M, Hornung S, Herrmann RG, Maier RM, Chiu WL, Sears B (2000) Complete nucleotide sequence of the Oenothera elata plastid chromosome, representing plastome I of the five distinguishable euoenothera plastomes. Mol Gen Genet 263:581–585

    CAS  PubMed  Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E et al (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136

    Article  CAS  PubMed  Google Scholar 

  • Kashino Y, Lauber WM, Carroll JA, Wang Q, Whitmars J, Satoh K, Pakrasi HB (2002) Proteomic analysis of a highly active photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides. Biochemistry 41:8004–8012

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi M, Katsuhiko O, Ikeuchi M (2005) A suppressor mutation in the phycocyanin gene in the light/glucose-sensitive phenotype of the psbk-disruptant of the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 46:1561–1567

    Article  CAS  PubMed  Google Scholar 

  • Koumandou VL, Nisbet RER, Barbrook AC, Howe CJ (2004) Dinoflagellate chloroplasts—where have all the genes gone? Trends Genet 20:261–267

    Article  CAS  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Lemieux C, Otis C, Turmel M (2000) Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution. Nature 403:649–652

    Article  CAS  PubMed  Google Scholar 

  • MacColl R (1998) Cyanobacterial phycobilisomes. J Struct Biol 124:311–334

    Article  CAS  PubMed  Google Scholar 

  • Makino A, Miyake C, Yokota A (2002) Physiological functions of the water–water cycle (Mehler reaction) and the cyclic electron flow around PSI in rice leaves. Plant Cell Physiol 43:1017–1026

    Article  CAS  PubMed  Google Scholar 

  • Mi H, Endo T, Ogawa T, Asada K (1995) Thylakoid membrane-bound, NADPH-specific pyridine nucleotide dehydrogenase complex mediates cyclic electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 36:661–668

    CAS  Google Scholar 

  • Molitor V, Peschek GA (1986) Respiratory electron transport in plasma and thylakoid membrane preparations from the cyanobacterium Anacystis nidulans. FEBS Lett 195:145–150

    Article  CAS  Google Scholar 

  • Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371

    Article  CAS  PubMed  Google Scholar 

  • Mäenpää P, Sippola K, Rokka A, Aro E-M (1998) Substitution of Ala-251 of the D1 reaction centre polypeptide with a charged residue results in impaired function of photosystem II. Plant Mol Biol 38:1191–2000

    Article  PubMed  Google Scholar 

  • O’Connor HE, Ruffle SV, Cain AJ, Deak Z, Vass I, Nugent JHA, Purton S (1998) The 9 kDa phosphoprotein of photosystem II. Generation and characterisation of Chlamydomonas mutants lacking PSII-H and a site-directed mutant lacking the phosphorylation site. Biochim Biophys Acta 1364:63–72

    Article  CAS  PubMed  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Rochaix JD (1997) Chloroplast reverse genetics: new insights into the function of plastid genes. Trends Plant Sci 2:419–425

    Article  Google Scholar 

  • Rokka A, Suorsa M, Saleem A, Battchikova N, Aro E-M (2005) Synthesis and assembly of thylakoid protein complexes: multiple assembly steps of photosystem II. Biochem J 388:159–168

    Article  CAS  PubMed  Google Scholar 

  • Ruf S, Kossel H, Bock R (2000) A small chloroplast-encoded protein as a novel architectural component of the light-harvesting antenna. J Cell Biol 139:95–102

    Article  Google Scholar 

  • Sato S, Nakamura Y, Kaneko T, Asamizu E, Tabata S (1999) Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res 6:283–290

    Article  CAS  PubMed  Google Scholar 

  • Scheller HV (1996) In vitro cyclic electron transport in barley thylakoids follows two independent pathways. Plant Physiol 110:187–194

    CAS  PubMed  Google Scholar 

  • Schluchter WM, Zhao J, Bryant DA (1993) Isolation and characterization of the ndhF gene of Synechococcus sp. PCC 7002 and initial characterization of an interposon mutant. J Bacteriol 175:3343–3352

    CAS  PubMed  Google Scholar 

  • Schägger H, von Jagow G (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379

    Article  PubMed  Google Scholar 

  • Sidler WA (1994) Phycobilisome and phycobiliprotein structures. In: Bryant DA (ed) The molecular biology of cyanobacteria. Kluwer Academic Publishers, The Netherlands, pp 139–216

    Google Scholar 

  • Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35:171–205

    CAS  PubMed  Google Scholar 

  • Swiatek M, Kuras R, Sokolenko A, Higgs D, Olive J, Cinque G, Muller B, Eichacker LA, Stern DB, Bassi R, Herrmann RG, Wollmann F-A (2001) The chloroplast gene ycf9 encodes a photosystem II (PSII) core subunit, PsbZ, that participates in PSII supramolecular architechture. Plant Cell 13:1347–1367

    Article  CAS  PubMed  Google Scholar 

  • Turmel M, Otis C, Lemieux C (1999) The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: insights into the architechture of ancestral chloroplast genomes. Proc Natl Acad Sci USA 96:10248–10253

    Article  CAS  PubMed  Google Scholar 

  • Tyystjärvi T, Aro E-M, Jansson C, Mäenpää P (1994) Changes of amino acid sequence in PEST-like area and QEEET motif affect degradation rate of D1 polypeptide in photosystem II. Plant Mol Biol 25:517–526

    Article  PubMed  Google Scholar 

  • Yao WB, Meng BY, Tanaka M, Sugiura M (1989) An additional promoter within the protein-coding region of the psbD–psbC gene cluster in tobacco chloroplast DNA. Nucleic Acids Res 17: 9583–9591

    Article  CAS  PubMed  Google Scholar 

  • Williams JGK (1988) Construction of specific mutations in the photosystem II photosynthetic reaction center by genetic engineering methods in the cyanobacterium Synechocystis 6803. Methods Enzymol 167:766–778

    Article  CAS  Google Scholar 

  • Zhang P, Battchikova N, Jansen T, Appel J, Ogawa T, Aro E-M (2004) Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp PCC 6803. Plant Cell 16:3326–3340

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Snyder WB, Muhlenhoff U, Rhiehl E, Warren PV, Goldbeck JH, Bryant DA (1993) Cloning and characterization of the psaE gene of the cyanobacterium Synechococcus sp. PCC 7002: characterization of a psaE mutant and overproduction of the protein in Escherichia coli. Mol Microbiol 9:1283–1294

    Article  Google Scholar 

Download references

Acknowledgements

The work in the U.K. was supported by funding from the U.K. Biotechnology and Biological Sciences Research Council and the Leverhulme Trust. The Finnish group acknowledges research grant from the Academy of Finland (PM), from Turku University Foundation (PM) and from CIMO (SU). We are grateful to Conrad Mullineaux for his advice and assistance with the 77 K fluorescence spectrometry and Yagut Allahverdiyeva for useful discussions.

Author information

Author notes

  1. Cleo L. Bishop

    Present address: Institute of Cellular and Molecular Sciences, Bart’s and the London Queen Mary’s School of Medicine and Dentistry, 4 Newark Street, London, E1 2AT, UK

  2. Elena Baena-Gonzalez

    Present address: Harvard Medical School, 25 Shattuck Street, Boston, MA, 02115, USA

Authors and Affiliations

  1. Photosynthesis Research Group, Department of Biology, University College London, Darwin Building, Gower Street, London, WC1E 6BT, UK

    Cleo L. Bishop, Saul Purton & Jonathan H. A. Nugent

  2. Department of Biology, Turku University, Turku, 20 014, Finland

    Simin Ulas, Elena Baena-Gonzalez, Eva-Mari Aro & Pirkko Mäenpää

Authors
  1. Cleo L. Bishop
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Simin Ulas
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Elena Baena-Gonzalez
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Eva-Mari Aro
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Saul Purton
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Jonathan H. A. Nugent
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Pirkko Mäenpää
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Pirkko Mäenpää.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bishop, C.L., Ulas, S., Baena-Gonzalez, E. et al. The PsbZ subunit of Photosystem II in Synechocystis sp. PCC 6803 modulates electron flow through the photosynthetic electron transfer chain. Photosynth Res 93, 139–147 (2007). https://doi.org/10.1007/s11120-007-9182-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-007-9182-0

Keywords