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Rethinking the existence of a steady-state Δψ component of the proton motive force across plant thylakoid membranes

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Abstract

Light-driven photosynthetic electron transport is coupled to the movement of protons from the chloroplast stroma to the thylakoid lumen. The resulting proton motive force that is generated is used to drive the conformational rotation of the transmembrane thylakoid ATPase enzyme which converts ADP (adenosine diphosphate) and Pi (inorganic phosphate) into ATP (adenosine triphosphate), the energy currency of the plant cell required for carbon fixation and other metabolic processes. According to Mitchell’s chemiosmotic hypothesis, the proton motive force can be parsed into the transmembrane proton gradient (ΔpH) and the electric field gradient (Δψ), which are thermodynamically equivalent. In chloroplasts, the proton motive force has been suggested to be split almost equally between Δψ and ΔpH (Kramer et al., Photosynth Res 60:151–163, 1999). One of the central pieces of evidence for this theory is the existence of a steady-state electrochromic shift (ECS) absorption signal detected ~515 nm in plant leaves during illumination. The interpretation of this signal is complicated, however, by a heavily overlap** absorption change ~535 nm associated with the formation of photoprotective energy dissipation (qE) during illumination. In this study, we present new evidence that dissects the overlap** contributions of the ECS and qE-related absorption changes in wild-type Arabidopsis leaves using specific inhibitors of the ΔpH (nigericin) and Δψ (valinomycin) and separately using leaves of the Arabidopsis lut2npq1 mutant that lacks qE. In both cases, our data show that no steady-state ECS signal persists in the light longer than ~60 s. The consequences of our observations for the suggesting parsing of steady-state thylakoid proton motive force between (ΔpH) and the electric field gradient (Δψ) are discussed.

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Acknowledgements

The authors wish to thank the Royal Society, the UK Biotechnology and Biological Sciences Research Council (BBSRC), and the Engineering and Physical Sciences Research council (EPSRC) for funding and Professor Peter Horton (University of Sheffield, UK) for very valuable discussions.

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  1. Department of Molecular Biology and Biotechnology, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK

    Matthew P. Johnson

  2. School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London, E1 4NS, UK

    Alexander V. Ruban

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Correspondence to Matthew P. Johnson.

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Johnson, M.P., Ruban, A.V. Rethinking the existence of a steady-state Δψ component of the proton motive force across plant thylakoid membranes. Photosynth Res 119, 233–242 (2014). https://doi.org/10.1007/s11120-013-9817-2

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