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D1-arginine257 mutants (R257E, K, and Q) of Chlamydomonas reinhardtii have a lowered QB redox potential: analysis of thermoluminescence and fluorescence measurements

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Abstract

Arginine257 (R257), in the de-helix that caps the QB site of the D1 protein, has been shown by mutational studies to play a key role in the sensitivity of Photosystem II (PS II) to bicarbonate-reversible binding of the formate anion. In this article, the role of this residue has been further investigated through D1 mutations (R257E, R257Q, and R257K) in Chlamydomonas reinhardtii. We have investigated the activity of the QB site by studying differences from wild type on the steady-state turnover of PS II, as assayed through chlorophyll (Chl) a fluorescence yield decay after flash excitation. The effects of p-benzoquinone (BQ, which oxidizes reduced QB, Q −B ) and 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU, which blocks electron flow from Q −A to QB) were measured. The equilibrium constants of the two-electron gate were obtained through thermoluminescence measurements. The thermoluminescence properties were changed in the mutants, especially when observed after pretreatment with 100 μM BQ. A theoretical analysis of the thermoluminescence data, based mainly on the recombination pathways model of Rappaport et al. (2005), led to the conclusion that the free-energy difference for the recombination of Q −B with S2 was reduced by 20–40 mV in the three mutants (D1-R257K, D1-R257Q, and D1-R257E); this was interpreted to be due to a lowering of the redox potential of QB/Q −B . Further, since the recombination of Q −A with S2 was unaffected, we suggest that no significant change in redox potential of QA/Q −A occurred in these three mutants. The maximum variable Chl a fluorescence yield is lowered in the mutants, in the order R257K > R257Q > R257E, compared to wild type. Our analysis of the binary oscillations in Chl a fluorescence following pretreatment of cells with BQ showed that turnover of the QB site was relatively unaffected in the three mutants. The mutant D1-R257E had the lowest growth rate and steady-state activity and showed the weakest binary oscillations. We conclude that the size and the charge of the amino acid at the position D1-257 play a role in PS II function by modulating the effective redox potential of the QB/Q −B pair. We discuss an indirect mechanism mediated through electrostatic and/or surface charge effects and the possibility of more pleiotropic effects arising from decreased stability of the D1/D2 and D1/CP47 interfaces.

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Abbreviations

BQ:

p-Benzoquinone

C. reinhardtii :

Chlamydomonas reinhardtii

Chl:

Chlorophyll

18-Crown-6:

Dicyclohexano-hexaoxacyclooctadecane

DCMU:

3-(3,4-Dichlorophenyl)-1,1-dimethylurea

DMBQ:

2,5-Dimethyl-p-benzoquinone

HS:

High salt culture medium

ms:

Millisecond(s)

PS II:

Photosystem II

Ph:

Pheophytin

QA :

Primary plastoquinone electron acceptor of Photosystem II

QB :

Secondary plastoquinone electron acceptor of Photosystem II

TAP:

Tris–acetate–phosphate culture medium

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Acknowledgments

Govindjee acknowledges support from the Department of Plant Biology, University of Illinois at Urbana-Champaign; ARC and SWR acknowledge support from NIH GM35438; JM acknowledges support from MEXT 18GS0318. MS acknowledges support from the Cooperative State Research, Education and Extension Service, U.S. Department of Agriculture, Project No. ILLU-875-389. We thank Jan Kern for discussions on the location of bicarbonate ions on the Photosystem II reaction center. We also thank George Papageorgiou for reading the final draft of this manuscript and for making valuable suggestions to improve the readability of this article.

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Author notes

  1. Jun Minagawa

    Present address: Institute of Low Temperature Science, Hokkaido University, Sapporo, 060-0819, Japan

  2. Manfredo Seufferheld

    Present address: Department of Natural Resources and Environmental Sciences (NRES), University of Illinois at Urbana-Champaign, 311 Edgar R. Madigan Lab (ERML), 1201 W. Gregory Drive, Urbana, IL, 61801, USA

  3. Bengt Svensson

    Present address: Department of Biochemistry, Molecular Biology and Biophysics, University of Minnesota, 6-155 Jackson Hall, 321 Church St. SE, Minneapolis, MN, 55455, USA

Authors and Affiliations

  1. Department of Biochemistry and Center for Biophysics and Computational Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Stuart Rose, Antony R. Crofts &  Govindjee

  2. Physiological and Molecular Plant Biology Program, University of Illinois at Urbana-Champaign, 286 Morrill Hall, 505 S. Goodwin Ave., Urbana, IL, 61801, USA

    Sean Padden

  3. Department of Chemistry, Princeton University, 17 Hoyt Laboratory, Washington Road, Princeton, NJ, 08544, USA

    Derrick R. J. Kolling

  4. Department of Plant Biology, University of Illinois at Urbana-Champaign, 265 Morrill Hall, 505 S. Goodwin Ave., Urbana, IL, 61801, USA

    Govindjee

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Jun Minagawa and Manfredo Seufferheld had equal credit in this work.

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Rose, S., Minagawa, J., Seufferheld, M. et al. D1-arginine257 mutants (R257E, K, and Q) of Chlamydomonas reinhardtii have a lowered QB redox potential: analysis of thermoluminescence and fluorescence measurements. Photosynth Res 98, 449–468 (2008). https://doi.org/10.1007/s11120-008-9351-9

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