Modeling of Fluorescence Quenching by Lutein in the Plant Light- Harvesting Complex LHCII C. D. P. Duffy,* ,† J. Chmeliov, ‡,§ M. Macernis, ‡,§ J. Sulskus, ‡ L. Valkunas, ‡,§ and A. V. Ruban † † The School of Biological and Chemical Sciences, Queen Mary, University of London, Mile End Road, London E1 4NS, U.K. ‡ Theoretical Physics Department, Faculty of Physics, Vilnius University, Saulė teko al. 9, LT-10222 Vilnius, Lithuania § Institute of Physics, Center for Physical Sciences and Technology, Gostauto 11, LT-01108 Vilnius, Lithuania * S Supporting Information ABSTRACT: Photoprotective non-photochemical quenching (NPQ) in higher plants is the result of the formation of energy quenching traps in the light-harvesting antenna of photosystem II (PSII). It has been proposed that this quenching trap is a lutein molecule closely associated with the chlorophyll terminal emitter of the major light-harvesting complex LHCII. We have used a combination of time-dependent density functional theory (TD-DFT) and the semiempirical MNDO-CAS-CI method to model the chlorophyll−lutein energy transfer dynamics of the highly quenched crystal structure of LHCII. Our calculations reveal that the incoherent “hopping” of energy from Chla612 to the short- lived, dipole forbidden 2 1 A g − state of lutein620 accounts for the strong fluorescence quenching observed in these crystals. This adds weight to the argument that the same dissipative pathway is responsible for in vivo NPQ. ■ INTRODUCTION Throughout natural history, one of the main challenges faced by photosynthetic organisms was living and evolving at very low levels of illumination, arising from life in aquatic environments, shading by competing organisms and other objects, cloud cover, etc. This selection pressure gave rise to the evolution of a light-harvesting antenna that is built of a number of pigment−protein complexes that serve to vastly enhance the spatial and spectral cross section of the reaction centers (RCs), the small, specific subset of chlorophylls responsible for photochemical charge separation. This arrangement ensures an optimal rate of energy delivery to the RCs despite low levels of illumination. However, as light exposure increases, particularly for the photosynthetic organisms that occupy land, this highly efficient antenna system can have a negative impact on the organism. The dangers posed by intense illumination arise from the fact that the maximum turnover rate of the RC is far slower than the rate of photon absorption and subsequent energy transfer in the antenna. Increasing illumination leads to a progressive saturation of the RCs. As more and more RCs are closed, there is a build-up of excitation energy within the antenna, leading to damage to photosystem II (PSII) which is particularly intense in the presence of oxygen. This damage, known as photoinhibition, 1 can take hours to reverse 2 and is seriously detrimental to the photosynthetic viability of the organism. However, evolutionary development has endowed some photosynthetic organisms, higher plants in particular, with the ability to cope with intense illumination through the collective action of many adaptive mechanisms. These mechanisms can deal with changes in light over a broad range of time scales, ranging from seasonal shifts to minute-by- minute fluctuations due to rapid changes in shading and cloud cover. For the most rapid fluctuations in light, this adaptation is made possible by the regulation of energy transduction in PSII by an enhancement of the nonradiative dissipation rate constant within the antenna. This regulation manifests itself as a decline in chlorophyll fluorescence yield of PSII in response to elevated illumination, a phenomenon known as non-photochemical quenching (NPQ). 3−7 The kinetics of NPQ formation and fluorescence recovery reveals several distinct components. The major component of NPQ is energy- dependent quenching (qE). qE normally forms in minutes in response to a rapid increase in illumination and relaxes equally quickly when light levels return to “normal”. It is the qE component of NPQ that represents the rapid photoprotective adaptation of the organism. Some slower components of NPQ also reflect photoprotective energy dissipation and could be due to the formation of zeaxanthin (qZ) and entrapment of protons within the quenched antenna. 8 The mentioned fast (qE) and slow photoprotective components of NPQ are frequently referred to as “photoprotective NPQ”. Another part of slowly reversible NPQ is attributed to the onset of photodamage− photoinhibitory quenching (qI). The qI component results from damage to a fraction of the RCs in PSII and can persist for several hours after the cessation of illumination. Essentially photoprotective NPQ arises from the formation of exciton- quenching trap sites within the antenna of PSII in high light. 9 These exciton-quenching sites capture excess excitation energy and dissipate it through some nonradiative process(es), thereby safely removing excess excitation energy from the antenna and reducing the excitation pressure felt by the RC. The phenomenon of photoprotective NPQ (pNPQ) and partic- Special Issue: Rienk van Grondelle Festschrift Received: July 24, 2012 Revised: December 11, 2012 Published: December 11, 2012 Article pubs.acs.org/JPCB © 2012 American Chemical Society 10974 dx.doi.org/10.1021/jp3110997 | J. Phys. Chem. B 2013, 117, 10974−10986