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An intact light harvesting complex I antenna system is required for complete state transitions in Arabidopsis

Nature Plants volume 1, Article number: 15176 (2015) Cite this article

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Abstract

Efficient photosynthesis depends on maintaining balance between the rate of light-driven electron transport occurring in photosystem I (PSI) and photosystem II (PSII), located in the chloroplast thylakoid membranes. Balance is achieved through a process of ‘state transitions’ that increases energy transfer towards PSI when PSII is overexcited (state II), and towards PSII when PSI is overexcited (state I). This is achieved through redox control of the phosphorylation state of light-harvesting antenna complex II (LHCII). PSI is served by both LHCII and four light-harvesting antenna complex I (LHCI) subunits, Lhca1, 2, 3 and 4. Here we demonstrate that despite unchanged levels of LHCII phosphorylation, absence of specific Lhca subunits reduces state transitions in Arabidopsis. The severest phenotype—observed in a mutant lacking Lhca4 (ΔLhca4)—displayed a 69% reduction compared with the wild type. Yet, surprisingly, the amounts of the PSI–LHCI–LHCII supercomplex isolated by blue native polyacrylamide gel electrophoresis (BN–PAGE) from digitonin-solubilized thylakoids were similar in the wild type and ΔLhca mutants. Fluorescence excitation spectroscopy revealed that in the wild type this PSI–LHCI–LHCII supercomplex is supplemented by energy transfer from additional LHCII trimers in state II, whose binding is sensitive to digitonin, and which are absent in ΔLhca4. The grana margins of the thylakoid membrane were found to be the primary site of interaction between this ‘extra’ LHCII and the PSI–LHCI–LHCII supercomplex in state II. The results suggest that the LHCI complexes mediate energetic interactions between LHCII and PSI in the intact membrane.

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Figure 1: State transitions and thylakoid protein phosphorylation in wild-type and ΔLhca plants.
Figure 2: Determination of PSI antenna size in wild-type and ΔLhca plants.
Figure 3: Effect of digitonin on PSI–LHCII interaction in wild-type and ΔLhca thylakoids.
Figure 4: PSI antenna size in wild-type grana and stromal lamellae membranes.

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Acknowledgements

M.P.J. acknowledges funding from the Leverhulme Trust (U.K.) and the Krebs Institute and Project Sunshine at the University of Sheffield. A.V.R. gratefully acknowledges funding from the Biotechnology and Biological Sciences Research Council (U.K.), Leverhulme Trust and The Royal Society Wolfson Research Merit Award. C.N.H. and M.P.J. acknowledge research grant BB/M000265/1 from the Biotechnology and Biological Sciences Research Council (UK). C.N.H. was also supported by an Advanced Award 338895 from the European Research Council. This work was also supported as part of the Photosynthetic Antenna Research Center (PARC), an Energy Frontier Research Center funded by the US Department of Energy, Office of Science, and Office of Basic Energy Sciences under Award Number DE-SC0001035. PARC's role was to provide partial support for C.N.H.

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  1. Samuel L. Benson & Pratheesh Maheswaran

    Present address: †Present addresses: Rothamsted Research, West Common, Harpenden, Hertfordshire AL5 2JQ, UK (S.L.B.); Allied Health Sciences Unit, Faculty of Medicine, University of Jaffna, Aadiyapatham Road, Kokuvil East, Kokuvil, Sri Lanka (P.M).,

Authors and Affiliations

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

    Samuel L. Benson, C. Neil Hunter, Peter Horton & Matthew P. Johnson

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

    Pratheesh Maheswaran, Maxwell A. Ware & Alexander V. Ruban

  3. Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, Umeå, SE-901 87, Sweden

    Stefan Jansson

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Contributions

S.L.B., P.M., M.A.W. and M.P.J. performed experiments. M.P.J. analysed the data. M.P.J, C.N.H., P.H., S.J. and A.V.R. designed the study and M.P.J. wrote the manuscript. All authors discussed the results and commented on the manuscript. P.H. and A.V.R. together carried out the preliminary experiments on which this study is based.

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Correspondence to Matthew P. Johnson.

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Benson, S., Maheswaran, P., Ware, M. et al. An intact light harvesting complex I antenna system is required for complete state transitions in Arabidopsis. Nature Plants 1, 15176 (2015). https://doi.org/10.1038/nplants.2015.176

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