Identification of a mechanism of photoprotective energy dissipation in higher plants

Under conditions of excess sunlight the efficient light-harvesting antenna(1) 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 heat(2,3), a process measured as the non-photochemical quenching of chlorophyll fluorescence or qE. Although the biological significance of qE is established(4-6), the molecular mechanisms involved are not(7-9). LHCII, the main light-harvesting complex, has an inbuilt capability to undergo transformation into a dissipative state by conformational change(10) 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 spectroscopy(11). 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 spectroscopy(12), 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.