Fluorescence lifetime analyses reveal how the high light-responsive protein LHCSR3 transforms PSII light-harvesting complexes into an energy-dissipative state [Bioenergetics]

In green algae, light-harvesting complex stress-related 3 (LHCSR3) is responsible for the pH-dependent dissipation of absorbed light energy, a function vital for survival under high-light conditions. LHCSR3 binds the photosystem II and light-harvesting complex II (PSII–LHCII) supercomplex and transforms it into an energy-dissipative form under acidic conditions, but the molecular mechanism remains unclear. Here we show that in the green alga Chlamydomonas reinhardtii, LHCSR3 modulates the excitation energy flow and dissipates the excitation energy within the light-harvesting complexes of the PSII supercomplex. Using fluorescence decay–associated spectra analysis, we found that, when the PSII supercomplex is associated with LHCSR3 under high-light conditions, excitation energy transfer from light-harvesting complexes to chlorophyll-binding protein CP43 is selectively inhibited compared with that to CP47, preventing excess excitation energy from overloading the reaction center. By analyzing femtosecond up-conversion fluorescence kinetics, we further found that pH- and LHCSR3-dependent quenching of the PSII—LHCII–LHCSR3 supercomplex is accompanied by a fluorescence emission centered at 684 nm, with a decay time constant of 18.6 ps, which is equivalent to the rise time constant of the lutein radical cation generated within a chlorophyll–lutein heterodimer. These results suggest a mechanism in which LHCSR3 transforms the PSII supercomplex into an energy-dissipative state and provide critical insight into the molecular events and characteristics in LHCSR3-dependent energy quenching.

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