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The nature of self-regulation in photosynthetic light-harvesting antenna

Nature Plants volume 2, Article number: 16045 (2016) Cite this article

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Abstract

The photosynthetic apparatus of green plants is well known for its extremely high efficiency that allows them to operate under dim light conditions. On the other hand, intense sunlight may result in overexcitation of the light-harvesting antenna and the formation of reactive compounds capable of ‘burning out’ the whole photosynthetic unit. Non-photochemical quenching is a self-regulatory mechanism utilized by green plants on a molecular level that allows them to safely dissipate the detrimental excess excitation energy as heat. Although it is believed to take place in the plant's major light-harvesting complexes (LHC) II, there is still no consensus regarding its molecular nature. To get more insight into its physical origin, we performed high-resolution time-resolved fluorescence measurements of LHCII trimers and their aggregates across a wide temperature range. Based on simulations of the excitation energy transfer in the LHCII aggregate, we associate the red-emitting state, having fluorescence maximum at ∼700 nm, with the partial mixing of excitonic and chlorophyll–chlorophyll charge transfer states. On the other hand, the quenched state has a totally different nature and is related to the incoherent excitation transfer to the short-lived carotenoid excited states. Our results also show that the required level of photoprotection in vivo can be achieved by a very subtle change in the number of LHCIIs switched to the quenched state.

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Figure 1: Time-resolved fluorescence measurements of LHCII aggregates at 150 K temperature.
Figure 2: Time-resolved fluorescence spectra of LHCII trimers.
Figure 3: Results of the decomposing time-resolved fluorescence spectra of LHCII aggregates, measured at various temperatures, in two major differently emitting components.
Figure 4: Model for excitation energy transfer in LHCII aggregate.
Figure 5: Origin of various conformational states of LHCII complexes and mean excitation lifetimes in small aggregates.

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Acknowledgements

This work was supported by the Research Council of Lithuania (LMT grant no. MIP-080/2015). Computations were performed using the resources of the High Performance Computing Center ‘HPC Sauletekis’ at the Faculty of Physics, Vilnius University. A.V.R. would like to acknowledge grants from The Leverhulme Trust and UK Biotechnology and Biological Sciences Research Council and The Royal Society for the Wolfson Research Merit Award. The authors also thank E. Belgio and P. Ungerer for the LHCII purification.

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Author notes

  1. Jevgenij Chmeliov and Andrius Gelzinis: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Theoretical Physics, Faculty of Physics, Vilnius University, Saulėtekio Avenue 9, LT-10222 Vilnius, Lithuania

    Jevgenij Chmeliov, Andrius Gelzinis & Leonas Valkunas

  2. Department of Molecular Compound Physics, Centre for Physical Sciences and Technology, Saulėtekio Avenue 3, LT-10222 Vilnius, Lithuania

    Jevgenij Chmeliov, Andrius Gelzinis, Egidijus Songaila, Ramūnas Augulis & Leonas Valkunas

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

    Christopher D. P. Duffy & Alexander V. Ruban

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Contributions

L.V. and A.V.R. designed the research. E.S. and R.A. performed the experiments. J.C. analysed experimental results in terms of self-modelling curve resolution, described high-temperature fluorescence kinetics in terms of fluctuating antenna model and made the figures of the manuscript. A.G. modelled excitation energy transfer in LHCII aggregates. L.V., R.A., J.C. and A.G. contributed to the interpretation of the experimental results. J.C. and A.G. wrote the manuscript. L.V., R.A., A.V.R. and C.D.P.D. discussed and commented on the manuscript.

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Correspondence to Leonas Valkunas.

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Chmeliov, J., Gelzinis, A., Songaila, E. et al. The nature of self-regulation in photosynthetic light-harvesting antenna. Nature Plants 2, 16045 (2016). https://doi.org/10.1038/nplants.2016.45

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