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The cytochrome b6f complex: plastoquinol oxidation and regulation of electron transport in chloroplasts

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Abstract

In oxygenic photosynthetic systems, the cytochrome b6f (Cytb6f) complex (plastoquinol:plastocyanin oxidoreductase) is a heart of the hub that provides connectivity between photosystems (PS) II and I. In this review, the structure and function of the Cytb6f complex are briefly outlined, being focused on the mechanisms of a bifurcated (two-electron) oxidation of plastoquinol (PQH2). In plant chloroplasts, under a wide range of experimental conditions (pH and temperature), a diffusion of PQH2 from PSII to the Cytb6f does not limit the intersystem electron transport. The overall rate of PQH2 turnover is determined mainly by the first step of the bifurcated oxidation of PQH2 at the catalytic site Qo, i.e., the reaction of electron transfer from PQH2 to the Fe2S2 cluster of the high-potential Rieske iron–sulfur protein (ISP). This point has been supported by the quantum chemical analysis of PQH2 oxidation within the framework of a model system including the Fe2S2 cluster of the ISP and surrounding amino acids, the low-potential heme b6L, Glu78 and 2,3,5-trimethylbenzoquinol (the tail-less analog of PQH2). Other structure–function relationships and mechanisms of electron transport regulation of oxygenic photosynthesis associated with the Cytb6f complex are briefly outlined: pH-dependent control of the intersystem electron transport and the regulatory balance between the operation of linear and cyclic electron transfer chains.

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Notes

  1. Here, the quinol oxidase site is defined as Qo, while this site is often nominated as Qp (see, for instance, Malone et al. (2021) and Sarewicz et al. (2021) and references therein).

Abbreviations

CBC:

The Calvin–Benson cycle

cryo-EM:

Cryogenic electron microscopy

Cyt:

Cytochrome

Cytb 6 f :

The Cyt b6f complex

DFT:

Density functional theory

EPR:

Electron paramagnetic resonance

ETC:

Electron transport chain

ISP:

The iron–sulfur protein

Fd:

Ferredoxin

FNR:

Ferredoxin-NADP-reductase

NDH-1:

NADH dehydrogenase-like complex type-1

PCET:

Proton-coupled electron transfer

PSI and PSII:

Photosystem I and photosystem II, respectively

Pc:

Plastocyanin

PQ, PSQ·, and PQH2 :

Plastoquinone (oxidized), plastosemiquinone, and plastoquinol (completely reduced) forms of plastoquinone; respectively

P700 :

Primary electron donor in PSI

ROS:

Reactive oxygen species

TDS:

Tridecyl-stigmatellin

TMBQH2 :

2,3,5-Trimethylbenzoquinol

WL:

White light

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Acknowledgements

This article is dedicated to the memory of Vladimir Shuvalov, an outstanding scientist who made fundamental contributions to elucidation of the mechanisms of electron transfer in photosynthetic systems. I would like to express my special acknowledgment to Dr. L.Yu. Ustynyuk for her decisive contribution to DFT modeling of a bifurcated oxidation of plastoquinol by the Cytb6f complex. I am deeply grateful to Drs. E.K. Ruuge, G.B. Khomutov, B.V. Trubitsin, and A.V. Vershubskii for fruitful collaboration in our earlier experimental and theoretical studies of regulatory processes in chloroplasts. I also thank the Reviewers for usefull and constructive comments.

Funding

This work was partly supported by the Russian Science Foundation (Grant 21-74-20047).

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  1. Department of Biophysics, Faculty of Physics, M.V. Lomonosov Moscow State University, Moscow, Russian Federation, 119991

    Alexander N. Tikhonov

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Tikhonov, A.N. The cytochrome b6f complex: plastoquinol oxidation and regulation of electron transport in chloroplasts. Photosynth Res 159, 203–227 (2024). https://doi.org/10.1007/s11120-023-01034-w

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