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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 S ₁ 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 S ₁ 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 S ₁ is an unlikely quenching mechanism, with pigment movements insufficiently pronounced to switch the system between quenched and unquenched states. Modulation of S ₁ 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 S ₁ oscillator strength and the real mechanism likely involves short-range interaction and/or non-trivial inter-molecular states.

SUBMITTER: Gray C

PROVIDER: S-EPMC8792765 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The dynamics of non-photochemical quenching (NPQ) of chlorophyll fluorescence and the dynamics of xanthophyll conversion under different actinic light conditions were studied in intact leaves of Arabidopsis thaliana. NPQ induction was investigated during up to 180 min illumination at 450, 900, and 1,800 ?mol photons m-2 s-1 (?E) and NPQ relaxation after 5, 30, 90, or 180 min of pre-illumination at the same light intensities. The comparison of wild-type plants with mutants affected either in xanthophyll conversion (npq1 and npq2) or PsbS expression (npq4 and L17) or lumen acidification (pgr1) indicated that NPQ states with similar, but not identical characteristics are induced at longer time range (15-60 min) in wild-type and mutant plants. In genotypes with an active xanthophyll conversion, the dynamics of two slowly (10-60 min) inducible and relaxing NPQ components were found to be kinetically correlated with zeaxanthin formation and epoxidation, respectively. However, the extent of NPQ was independent of the amount of zeaxanthin, since higher NPQ values were inducible with increasing actinic light intensities without pronounced changes in the zeaxanthin amount. These data support an indirect role of zeaxanthin in pH-independent NPQ states rather than a specific direct function of zeaxanthin as quencher in long-lasting NPQ processes. Such an indirect function might be related to an allosteric regulation of NPQ processes by zeaxanthin (e.g., through interaction of zeaxanthin at the surface of proteins) or a general photoprotective function of zeaxanthin in the lipid phase of the membrane (e.g., by modulation of the membrane fluidity or by acting as antioxidant). The found concomitant down-regulation of zeaxanthin epoxidation and recovery of photosystem II activity ensures that zeaxanthin is retained in the thylakoid membrane as long as photosystem II activity is inhibited or down-regulated. This regulation supports the view that zeaxanthin can be considered as a kind of light stress memory in chloroplasts, allowing a rapid reactivation of photoprotective NPQ processes in case of recurrent light stress periods.

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

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