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Reaction centers from three herbicide resistant mutants of Rhodobacter sphaeroides 2.4.1: Kinetics of electron transfer reactions

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Abstract

Electron transfer rates were measured in RCs from three herbicide-resistant mutants with known amino acid changes to elucidate the structural requirements for last electron transfer. The three herbicide resistant mutants were IM(L229) (Ile-L229↦ Met), SP(L223) (Ser-L223↦ Pro) and YG(L222) (Tyr-L222↦ Gly). The electron transfer rate D+QA -QB↦D+QAQB (k AB) is slowed ∼3 fold in the IM(L229) and YG(L222) RCs (pH 8). The stabilization of D+QAQB - with respect to D+QAQB - (pH 8) was found to be eliminated in the IM(L229) mutant RCs (ΔG0 ∼ 0 meV), was partially reduced in the SP(L223) mutant RCs (ΔG0=−30 meV), and was unaltered in the YG(L222) mutant RCs (ΔG0=−60 meV), compared to that observed in the native RCs (ΔG0=−60 meV). The pH dependences of the charge recombination rate D+QAQB -↦DQAQB (k BD) and the electron transfer from QA - (k QA -↦QA) suggest that the mutations do not affect the protonation state of Glu-L212 nor the electrostatic interactions of QB and QB - with Glu-L212. The binding affinities of UQ10 for the QB site were found in order of decreasing values to be native ≥IM(L229) > YG(L222)≥ SP(L223). The altered properties of the mutant RCs are used to deduce possible structural changes caused by the mutations and are dicscussed in terms of photosynthetic efficiency of the herbicide resistant strains.

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Abbreviations

Bchl:

bacteriochlorophyll

Bphe:

bacteriopheophytin

cholate:

3α,7α,12α-trihydroxycholanic acid

D:

donor (bacteriochlorophyll dimer)

EDTA:

ethylenediamine tetraacetic acid

Fe2+ :

non-heme iron atom

LDAO:

lauryl dimethylamine oxide

PS II:

photosystem II

QA and QB :

primary and secondary quinone acceptors

RC:

bacterial reaction center

Tris:

tris(hydroxymethyl)aminomethane

UQ0 :

2,3-dimethoxy-5-methyl benzoquinone

UQ10 :

ubiquinone 50

References

  • Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1988) Structure of the reaction center from Rhodobacter sphaeroides R-26: protein-cofactor (quinones and Fe2+) interactions. Proc Natl Acad Sci USA 85: 8487–8491

    PubMed  Google Scholar 

  • Bowes J, Crofts AR and Arntzen CJ (1980) Redox reactions on the reducing side of photosystem II in chloroplasts with altered herbicide binding properties. Archiv Biochim Biophys 200: 303–308

    Google Scholar 

  • Breton J and Vermeglio A (eds) (1988) The Photosynthetic Bacterial Reaction Center: Structure and Dynamics. Plenum, New York

    Google Scholar 

  • Brown AE, Gilbert CW, Guy R and Arntzen CJ (1984) Triazine herbicide resistance in the photosynthetic bacterium Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 81: 6310–6314

    Google Scholar 

  • Bylina EJ, Jovine RVM and Youvan DC (1989) A genetic system for rapidly assessing herbicides that compete for the quinone binding site of photosynthetic reaction centers. Bio/Technology 7: 69–74

    Article  Google Scholar 

  • Etienne AL, Astier C, Ailani G, Kirilovsky D, Ducreut JM and Vernotte C (1990) Comparative studies of herbicide resistant mutants of Synechocystis 6714 and of higher plants. Proceedings from the VIIIth International Congress on Photosynthesis, I.2.543–I.2.546

  • Ewald G, Wiessner C and Michel H (1990) Sequence analysis of four atrazine-resistant mutants from Rhodopseudomonas viridis. Z Naturforsch 45C: 459–462

    Google Scholar 

  • Feher G and Okamura MY (1978) Chemical composition and properties of reaction centers. In: Clayton RK and Sistrom WR (eds) The Photosynthetic Bacteria, pp 349–386. New York: Plenum Press

    Google Scholar 

  • Giangiacomo KM and Dutton PL (1989) Temperature and free energy dependence of electron transfer kinetics between quinones bound at the QA and QB sites in photosynthetic reaction centers from Rhodobacter sphaeroides (Abstract). Biophys J 55: 179a

  • Gilbert CW, Williams JGK, Williams KAL and Arntzen CJ (1985) Herbicide action in photosynthetic bacteria. In: Steinbeck KE, Bonitz S, Arntzen CJ and Bogorad L (eds) Molecular Biology of the Photosynthetic Apparatus, pp 67–71. Cold Spring Harbor: Cold Spring Harbor Laboratory

    Google Scholar 

  • Golden SS and Haselkorn R (1985) Mutation to herbicide resistance maps within the psbA gene of Anacystis nidulans R2. Science 229: 1104–1107

    PubMed  Google Scholar 

  • Hirschberg J and McIntosh L (1983) Molecular basis of herbicide resistance in Amaranthus hybridus. Science 222: 1346–1349

    Google Scholar 

  • Kleinfeld D, Okamura MY and Feher G (1984) Electron transfer in reaction centers of Rhodopseudomonas sphaeroides. Determination of the charge recombination pathway of D+QAQB - and free energy and kinetic relations between QA -QB and QAQB -. Biochim Biophys Acta 766: 126–140

    PubMed  Google Scholar 

  • Marcus RA and Sutin N (1985) Electron transfer in chemistry and biology. Biochim Biophys Acta 811: 265–322

    Google Scholar 

  • McPherson PH, Okamura MY and Feher G (1990) Electron transfer from the reaction center of Rb. sphaeroides to the quinone pool: doubly reduced QB leaves the reaction center. Biochim Biophys Acta 1016: 289–292

    Google Scholar 

  • Michel H and Deisenhofer J (1988) Relevance of the photosynthetic reaction center from purple bacteria to the structure of photosystem II. Biochem 27: 1–7

    Google Scholar 

  • Michel H, Epp O and Deisenhofer J (1986) Pigment-protein interactions in the photosynthetic reaction centre from Rhodopseudomonas viridis. EMBO J 5: 2445–2451

    Google Scholar 

  • Ort DR, Ahrens WH, Martin B and Stoller EW (1983) Comparison of photosynthetic performance in triazine-resistant and susceptible biotypes of Amaranthus hybridus. Plant Physiol 72: 925–930

    Google Scholar 

  • Paddock ML, McPherson PH, Feher G and Okamura MY (1990) Pathway of proton transfer in bacterial reaction centers: replacement of serine-L223 by alanine inhibits electron and proton transfers associated with the reduction of quinone to dihydroquinone. Proc Natl Acad Sci USA 87: 6803–6807

    PubMed  Google Scholar 

  • Paddock ML, Rongey SH, Abresch EC, Feher G and Okamura MY (1988) Reaction centers from three herbicideresistant mutants of Rhodobacter sphaeroides 2.4.1: sequence analysis and preliminary characterization. Photosynth Res 17: 75–96

    Google Scholar 

  • Paddock ML, Rongey SH, Feher G and Okamura MY (1989) Pathway of proton transfer in bacterial reaction centers: replacement of glutamic acid 212 in the L subunit by glutamine inhibits quinone (secondary acceptor) turnover. Proc Natl Acad Sci USA 86: 6602–6606

    PubMed  Google Scholar 

  • Schenck CC, Sistrom WR and Capaldi RA (1986) Structurefunction studies in reaction centers: characterization of an herbicide resistance mutation in Rhodopseudomonas sphaeroides (Abstract). Biophys J 49: 486a

  • Sinning I, Michel H, Mathis P and Rutherford AW (1989) Characterization of four herbicide-resistant mutants of Rhodopseudomonas viridis by genetic analysis, electron paramagnetic resonance, and optical spectroscopy. Biochem 28: 5544–5553

    Google Scholar 

  • Stein RR, Castellvi AL, Bogacz JP and Wraight CA (1984) Herbicide-quinone competition in the acceptor complex of photosynthetic reaction centers from Rhodopseudomonas sphaeroides: a bacterial model for PS-II-herbicide activity in plants. J Cell Biochem 24: 243–259

    PubMed  Google Scholar 

  • Takahashi E, Maroti P and Wraight C (1990) Site-directed mutagenesis of the Rhodobacter sphaeroides reaction center: the role of tyrosine L222. Proceedings from the VIIIth International Congress on Photosynthesis, I.1.169–I.1.172

  • Taoka S and Crofts AR (1990) Two electron gate in triazine resistant and susceptible Amaranthus hybridus. Proceedings from the VIIIth International Congress on Photosynthesis, I.2.547–I.2.550

  • Trebst A (1987) The three-dimensional structure of the herbicide binding niche on the reaction center polypeptides from photosystem II. Z Naturforsch 42c: 742–750

    Google Scholar 

  • Velthuys BR (1981) Electron-dependent competition between plastoquinone and inhibitors for binding to photosystem II. FEBS Lett 126: 277–281

    Article  Google Scholar 

  • Vermeglio A and Clayton RK (1977) Kinetics of electron transfer between the primary and the secondary acceptor in reaction centers from Rhodopseudomonas sphaeroides. Biochim Biophys Acta 461: 159–165

    PubMed  Google Scholar 

  • Wraight CA (1981) Oxidation-reduction physical chemistry of the acceptor quinone complex in bacterial photosynthetic reaction centers: evidence for a new model of herbicide activity. Israel J Chem 21: 348–354

    Google Scholar 

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Authors and Affiliations

  1. Department of Physics, B-019, University of California, San Diego, 92093, La Jolla, CA, USA

    Mark L. Paddock, George Feher & Melvin Y. Okamura

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  1. Mark L. Paddock
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  2. George Feher
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  3. Melvin Y. Okamura
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Paddock, M.L., Feher, G. & Okamura, M.Y. Reaction centers from three herbicide resistant mutants of Rhodobacter sphaeroides 2.4.1: Kinetics of electron transfer reactions. Photosynth Res 27, 109–119 (1991). https://doi.org/10.1007/BF00033250

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  • DOI: https://doi.org/10.1007/BF00033250

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