Identification of a mechanism of photoprotective energy dissipation in higher plants

Identification of a mechanism of photoprotective energy dissipation in higher plants

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ABSTRACT Under conditions of excess sunlight the efficient light-harvesting antenna1 found in the chloroplast membranes of plants is rapidly and reversibly switched into a photoprotected


quenched state in which potentially harmful absorbed energy is dissipated as heat2,3, a process measured as the non-photochemical quenching of chlorophyll fluorescence or qE. Although the


biological significance of qE is established4,5,6, the molecular mechanisms involved are not7,8,9. LHCII, the main light-harvesting complex, has an inbuilt capability to undergo


transformation into a dissipative state by conformational change10 and it was suggested that this provides a molecular basis for qE, but it is not known if such events occur _in vivo_ or how


energy is dissipated in this state. The transition into the dissipative state is associated with a twist in the configuration of the LHCII-bound carotenoid neoxanthin, identified using


resonance Raman spectroscopy11. Applying this technique to study isolated chloroplasts and whole leaves, we show here that the same change in neoxanthin configuration occurs _in vivo_, to an


extent consistent with the magnitude of energy dissipation. Femtosecond transient absorption spectroscopy12, performed on purified LHCII in the dissipative state, shows that energy is


transferred from chlorophyll _a_ to a low-lying carotenoid excited state, identified as one of the two luteins (lutein 1) in LHCII. Hence, it is experimentally demonstrated that a change in


conformation of LHCII occurs _in vivo_, which opens a channel for energy dissipation by transfer to a bound carotenoid. We suggest that this is the principal mechanism of photoprotection.


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support SIMILAR CONTENT BEING VIEWED BY OTHERS THE NATURE OF CAROTENOID S* STATE AND ITS ROLE IN THE NONPHOTOCHEMICAL QUENCHING OF PLANTS Article Open access 29 January 2024 ULTRAFAST ENERGY


QUENCHING MECHANISM OF LHCSR3-DEPENDENT PHOTOPROTECTION IN _CHLAMYDOMONAS_ Article Open access 24 May 2024 LIGHT-HARVESTING COMPLEX II IS AN ANTENNA OF PHOTOSYSTEM I IN DARK-ADAPTED PLANTS


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fluorescence quenching in the absence of zeaxanthin. _FEBS Lett._ 580, 2053–2058 (2006) Article  CAS  Google Scholar  Download references ACKNOWLEDGEMENTS This work was supported by grants


from: UK Biotechnology and Biological Sciences Research Council (P.H., A.V.R.); the Netherlands Organization for Scientific Research via the Foundation of Earth and Life Sciences (R.v.G.,


H.v.A., J.T.M.K., R.B.) and a VIDI Fellowship (J.T.M.K); Laserlab Europe; ANR (program caroprotect) (A.A.P., B.R.); and the INTRO2 EU FP6 Marie Curie Research Training Network. We thank K.


K. Niyogi for the gift of seeds of the L17 _Arabidopsis_ line. AUTHOR INFORMATION Author notes * Alexander V. Ruban and Rudi Berera: These authors have contributed equally to this work.


AUTHORS AND AFFILIATIONS * School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK , Alexander V. Ruban * Department of Physics and


Astronomy, Faculty of Sciences, VU University Amsterdam, De Boelelaan 1081, 1081 HV Amsterdam, The Netherlands, Rudi Berera, Ivo H. M. van Stokkum, John T. M. Kennis & Rienk van


Grondelle * Commissariat à l'Energie Atomique (CEA), Institut de Biologie et Technologies de Saclay (iBiTecS) and Centre National de la Recherche Scientifique (CNRS), Gif-sur-Yvette,


F-91191, France , Cristian Ilioaia, Andrew A. Pascal & Bruno Robert * Department of Molecular Biology and Biotechnology, University of Sheffield, Western Bank, Sheffield S10 2TN, UK,


Cristian Ilioaia & Peter Horton * Laboratory of Biophysics, Wageningen University, PO Box 8128, 6700 ET, Wageningen, The Netherlands , Herbert van Amerongen Authors * Alexander V. Ruban


View author publications You can also search for this author inPubMed Google Scholar * Rudi Berera View author publications You can also search for this author inPubMed Google Scholar *


Cristian Ilioaia View author publications You can also search for this author inPubMed Google Scholar * Ivo H. M. van Stokkum View author publications You can also search for this author


inPubMed Google Scholar * John T. M. Kennis View author publications You can also search for this author inPubMed Google Scholar * Andrew A. Pascal View author publications You can also


search for this author inPubMed Google Scholar * Herbert van Amerongen View author publications You can also search for this author inPubMed Google Scholar * Bruno Robert View author


publications You can also search for this author inPubMed Google Scholar * Peter Horton View author publications You can also search for this author inPubMed Google Scholar * Rienk van


Grondelle View author publications You can also search for this author inPubMed Google Scholar CORRESPONDING AUTHORS Correspondence to Bruno Robert, Peter Horton or Rienk van Grondelle.


SUPPLEMENTARY INFORMATION SUPPLEMENTARY INFORMATION This file contains Supplementary Figures 1-6 with Legends and Table 1. The file describes additional supportive data. Firstly, Raman


spectra used to determine the contribution of the neoxanthin signal to the in vivo spectra, and the spectra obtained for various LHCII sample in different quenching states. Secondly, further


transient absorption traces are displayed, including those recorded in the IR region, and those obtained for LHCII sample at an intermediate quenching state. A more complete description of


the model used to fit the absorption data is described, along with a table of all rate constants. (PDF 553 kb) RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS


ARTICLE Ruban, A., Berera, R., Ilioaia, C. _et al._ Identification of a mechanism of photoprotective energy dissipation in higher plants. _Nature_ 450, 575–578 (2007).


https://doi.org/10.1038/nature06262 Download citation * Received: 30 April 2007 * Accepted: 14 September 2007 * Issue Date: 22 November 2007 * DOI: https://doi.org/10.1038/nature06262 SHARE


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