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Identification of a mechanism of photoprotective energy dissipation in higher plants

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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Figure 1: Quenching-related changes in the neoxanthin region of the resonance Raman spectrum of isolated LHCII, chloroplasts and leaves.
Figure 2: Femtosecond spectroscopy of LHCII in the unquenched and quenched states.
Figure 3: Model illustrating the molecular mechanism of qE.

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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.

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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)

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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

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