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Photodamage of iron–sulphur clusters in photosystem I induces non-photochemical energy dissipation

Nature Plants volume 2, Article number: 16035 (2016) Cite this article

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Abstract

Photosystem I (PSI) uses light energy and electrons supplied by photosystem II (PSII) to reduce NADP+ to NADPH. PSI is very tolerant of excess light but extremely sensitive to excess electrons from PSII. It has been assumed that PSI is protected from photoinhibition by strict control of the intersystem electron transfer chain (ETC). Here we demonstrate that the iron–sulphur (FeS) clusters of PSI are more sensitive to high light stress than previously anticipated, but PSI with damaged FeS clusters still functions as a non-photochemical photoprotective energy quencher (PSI-NPQ). Upon photoinhibition of PSI, the highly reduced ETC further triggers thylakoid phosphorylation-based mechanisms that increase energy flow towards PSI. It is concluded that the sensitivity of FeS clusters provides an additional photoprotective mechanism that is able to downregulate PSII, based on PSI quenching and protein phosphorylation.

PSI is very tolerant against excess energy and has been reported to become damaged only under very specific stress conditions when the transfer of electrons to PSI exceeds the capacity of the PSI electron acceptors1–4. PSI photoinhibition was initially described as an oxidative destruction of the FeS clusters of PSI in chilling sensitive cucumber plants because of inactivation of superoxide dismutase3. More recently, evidence has accumulated indicating that PSI is more susceptible to damage than PSII under fluctuating light conditions5,6. Depending on the phylogenetic position inside the green lineage, oxygenic photosynthetic organisms have evolved with different mechanisms to protect PSI against photodamage, either by limiting electron transfer to PSI or by providing an alternative limitless sink for the electrons7.

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Figure 1: Redox kinetics of PSI when shifting the WT and pgr5 plants from growth light to high light for indicated time periods.
Figure 2: Room temperature EPR spectra from thylakoid membranes from WT and the pgr5 mutant.
Figure 3: Reduction of the FA and FB centres of PSI in the thylakoid membrane at 16 K.
Figure 4: Fluorescence emission spectra from WT and the pgr5 plants.
Figure 5: Gaussian decomposition of low temperature fluorescence emission spectra at 0 min and 120 min high-light-treated thylakoids of WT and pgr5.
Figure 6: Schematic representation of the regulatory functions of PSI in the presence (WT plants) and absence (pgr5 mutant) of ΔpH-dependent control mechanisms.

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Acknowledgements

Research was financially supported by the Academy of Finland Center of Excellence project (271832), a post-doctoral research grant to M.T. (260094) and an Academy Professor research grant to E.-M.A. (273870). S.S. and F.M. thankfully acknowledge the Swedish Research Council, the Swedish Energy Agency and the Knut and Alice Wallenberg Foundation. The PsaD antibody is a kind gift from H. Vibe Scheller, and the pgr5 mutant and the gl1 wild-type control were kindly provided by T. Shikanai.

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Author notes

  1. Michele Grieco & Anjana Jajoo

    Present address: †Present addresses: Department of Ecogenomics and Molecular Systems Biology (MoSys), University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria (M.G.); School of Life Sciences, Devi Ahilya University, Indore 452001, Madhya Pradesh, India (A.J.).,

Authors and Affiliations

  1. Department of Biochemistry, Molecular Plant Biology, University of Turku, FI-20014 Turku, Finland

    Arjun Tiwari, Michele Grieco, Marjaana Suorsa, Anjana Jajoo, Mikko Tikkanen & Eva-Mari Aro

  2. Department of Chemistry-Ångström Laboratory, Molecular Biomimetics, Uppsala University, Box 523, SE-75120 Uppsala, Sweden

    Fikret Mamedov & Stenbjörn Styring

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Contributions

A.T., M.T., M.S., A.J. and E.-M.A. designed the study; A.T. and F.M. performed the research; A.T., F.M. and M.G. contributed analytical tools; A.T., M.T., S.S., F.M. and E.-M.A. analysed the data; A.T., F.M., M.T., M.S. and E.-M.A. wrote the paper.

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Correspondence to Mikko Tikkanen or Eva-Mari Aro.

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Tiwari, A., Mamedov, F., Grieco, M. et al. Photodamage of iron–sulphur clusters in photosystem I induces non-photochemical energy dissipation. Nature Plants 2, 16035 (2016). https://doi.org/10.1038/nplants.2016.35

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