Zeaxanthin Protects Plant Photosynthesis by Modulating Chlorophyll Triplet Yield in Specific Light-harvesting Antenna Subunits

Abstract

Background:The plant carotenoid zeaxanthin is accumulated under excess light.Results: Zeaxanthin induces a red shift in the carotenoid triplet excited state spectrum and reveals a higher efficiency in controlling chlorophyll triplet formation. Conclusion:Binding of zeaxanthin to specific proteins modulates the yield of dangerous chlorophyll excited states and protects photosynthesis from over-excitation.Significance: Functional dissection of zeaxanthin-dependent photoprotective mechanisms is crucial for understanding how plants avoid photoinhibition.Plants are particularly prone to photo-oxidative damage caused by excess light.Photoprotection is essential for photosynthesis to proceed in oxygenic environments either by scavenging harmful reactive intermediates or preventing their accumulation to avoid photoinhibition.Carotenoids play a key role in protecting photosynthesis from the toxic effect of over-excitation; under excess light conditions, plants accumulate a specific carotenoid, zeaxanthin, that was shown to increase photoprotection.In this work we genetically dissected different components of zeaxanthin-dependent photoprotection.By using time-resolved differential spectroscopy in vivo, we identified a zeaxanthin-dependent optical signal characterized by a red shift in the carotenoid peak of the triplet-minus-singlet spectrum of leaves and pigment-binding proteins.By fractionating thylakoids into their component pigment binding complexes, the signal was found to originate from the monomeric Lhcb4 -6 antenna components of Photosystem II and the Lhca1-4 subunits of Photosystem I.By analyzing mutants based on their sensitivity to excess light, the red-shifted triplet-minussinglet signal was tightly correlated with photoprotection in the chloroplasts, suggesting the signal implies an increased efficiency of zeaxanthin in controlling chlorophyll triplet formation.Fluorescence-detected magnetic resonance analysis showed a decrease in the amplitude of signals assigned to chlorophyll triplets belonging to the monomeric antenna complexes of Photosystem II upon zeaxanthin binding; however, the amplitude of carotenoid triplet signal does not increase correspondingly.Results show that the high light-induced binding of zeaxanthin to specific proteins plays a major role in enhancing photoprotection by modulating the yield of potentially dangerous chlorophyll-excited states in vivo and preventing the production of singlet oxygen.