Trivial Excitation Energy Transfer to Carotenoids Is an Unlikely Mechanism for Non-photochemical Quenching in LHCII

Abstract

Higher plants defend themselves from bursts of intense light via the mechanism of Non-Photochemical Quenching (NPQ). It involves the Photosystem II (PSII) antenna protein (LHCII) adopting a conformation that favors excitation quenching. In recent years several structural models have suggested that quenching proceeds via energy transfer to the optically forbidden and short-lived S1 states of a carotenoid. It was proposed that this pathway was controlled by subtle changes in the relative orientation of a small number of pigments. However, quantum chemical calculations of S1 properties are not trivial and therefore its energy, oscillator strength and lifetime are treated as rather loose parameters. Moreover, the models were based either on a single LHCII crystal structure or Molecular Dynamics (MD) trajectories about a single minimum. Here we try and address these limitations by parameterizing the vibronic structure and relaxation dynamics of lutein in terms of observable quantities, namely its linear absorption (LA), transient absorption (TA) and two-photon excitation (TPE) spectra. We also analyze a number of minima taken from an exhaustive meta-dynamical search of the LHCII free energy surface. We show that trivial, Coulomb-mediated energy transfer to S1 is an unlikely quenching mechanism, with pigment movements insufficiently pronounced to switch the system between quenched and unquenched states. Modulation of S1 energy level as a quenching switch is similarly unlikely. Moreover, the quenching predicted by previous models is possibly an artifact of quantum chemical over-estimation of S1 oscillator strength and the real mechanism likely involves short-range interaction and/or non-trivial inter-molecular states.

Impact of structural sampling, coupling scheme and state of interest on the energy transfer in CP29

“…There are plenty of postulated mechanisms, especially for the LHCII. [50][51][52][53][54] Many, but not all of these proposals require Crts.…”

Low-Lying Excited States of Natural Carotenoids Viewed by Ab Initio Methods

“…On the other hand, the 2A g – state acts as an acceptor of excitation energy from the low-energy cluster of chlorophylls. ,− The 2A g – state undergoes rapid radiationless decay, thus serving as a sink for excessive excitation energy under high-illumination conditions. While the latter mechanism has been questioned recently, it remains one of the most probable pathways for the non-photochemical quenching of chlorophyll fluorescence, although it is probably not a trivial excitation energy transfer. However, the mechanism should involve energy transfer to the 2A g – state in some way, since an alternative dissipation pathway involving the formation of a cation–radical chlorophyll–lutein pair has only limited evidence based on rather weak computational arguments or experiments showing only a small fraction of this pathway …”

PeVDE, a violaxanthin de-epoxidase gene from moso bamboo, confers photoprotection ability in transgenic Arabidopsis under high light

“…Although light is essential for photosynthesis, excessive light can cause oxidative damage to the photosynthetic apparatus by producing reactive oxygen species (ROS) ( Müller et al, 2001 ; Takahashi and Badger, 2011 ). To prevent oxidative damage to the photosynthetic apparatus, plants have developed a series of photoprotection mechanisms ( Goss and Lepetit, 2015 ; Leonelli et al, 2017 ; Velitchkova et al, 2020 ; Gray et al, 2022 ). One of the most rapid and efficient protection mechanisms is dissipating the excess absorbed light energy as thermal energy, which can be monitored as the non-photochemical quenching (NPQ) of chlorophyll fluorescence ( Jahns and Holzwarth, 2012 ; Goss and Lepetit, 2015 ; Ruban and Wilson, 2021 ).…”