On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls

Selective 2-photon excitation (TPE) of carotenoid dark states, Car S-1, shows that in the major light-harvesting complex of photosystem II (LHCII), the extent of electronic interactions between carotenoid dark states (Car S1) and chlorophyll (Chl) states, phi(CarS1-Chl)(Coupling), correlates linearly with chlorophyll fluorescence quenching under different experimental conditions. Simultaneously, a linear correlation between both Chl fluorescence quenching and phi(CarS1-Chl)(Coupling) with the intensity of red-shifted bands in the Chl Qy and carotenoid absorption was also observed. These results suggest quenching excitonic Car S-1-Chl states as origin for the observed effects. Furthermore, real time measurements of the light-dependent down-and up-regulation of the photosynthetic activity and phi(CarS1-Chl)(Coupling) in wild-type and mutant (npq1, npq2, npq4, lut2 and WT + PsbS) Arabidopsis thaliana plants reveal that also in vivo the quenching parameter NPQ correlates always linearly with the extent of electronic Car S-1-Chl interactions in any adaptation status. Our in vivo measurements with Arabidopsis variants show that during high light illumination, phi(CarS1-Chl)(Coupling) depends on the presence of PsbS and zeaxanthin (Zea) in an almost identical way as NPQ. In summary, these results provide clear evidence for a very close link between electronic Car S-1-Chl interactions and the regulation of photosynthesis. These findings support a photophysical mechanism in which short-living, low excitonic carotenoid chlorophyll states serve as traps and dissipation valves for excess excitation energy.