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

Callum Gray,Tomáš Polívka,Tiejun Wei,Vangelis Daskalakis,Christopher D P Duffy

doi:10.3389/fpls.2021.797373

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.

Highlights

Non-photochemical quenching (NPQ) in higher plants is a regulatory response to a sudden increase in light intensity (Horton et al, 2000; Niyogi, 2000; Müller et al, 2001; Ruban et al, 2012)
We do not calculate the Chl excitation energies in situ but take the average values reported in Müh et al (2010)
We are not saying that the different minima do not represent different functional states or that carotenoids are not involved in quenching, merely that our model does not capture its key features

Summary

Introduction

Non-photochemical quenching (NPQ) in higher plants is a regulatory response to a sudden increase in light intensity (Horton et al, 2000; Niyogi, 2000; Müller et al, 2001; Ruban et al, 2012) It is a (mostly Malnoë et al, 2018) reversible down-regulation of the quantum efficiency of the Photosystem II (PSII) lightharvesting antenna (LHCII) with the purpose of defending the saturated reaction centers from over-excitation and photoinhibition (Powles, 1984; Aro et al, 1993). Either way (for further information, the reader is directed to a comprehensive review of this complex and ongoing topic Ruban, 2016) the combined effect is to induce an in-membrane aggregation or clustering of LHCII (Horton et al, 1991) and some subtle internal conformational changes (Ilioaia et al, 2011) These somehow modulate the pigment-pigment and pigment-protein couplings to create a quenching species, the nature of the quencher and molecular dynamics of the conformational “switch” are still unclear

Methods

Results

Conclusion