Energy-dependent quenching adjusts the excitation diffusion length to regulate photosynthetic light harvesting

Abstract

SignificancePlants’ photosynthetic mechanism adjusts to fluctuations in light intensity. Intermittent bright sunlight can damage light-harvesting proteins; to preempt this, plants dissipate excess absorbed excitation energy as heat. Energy-dependent quenching (qE) of excitations occurs on the seconds to minutes timescale through conformational changes in antenna proteins. Using a multiscale model of photosystem II, we show that changes in light harvesting due to qE can be explained using a single parameter, the excitation diffusion length, which decreases as qE activates. These findings have implications for the interpretation of pulse amplitude-modulated fluorescence, a common noninvasive measurement of photosynthetic activity in leaves.

Chlorophyll–carotenoid excitation energy transfer and charge transfer in Nannochloropsis oceanica for the regulation of photosynthesis

“…An NPQ value (NPQτ) of 6 suggests that the Zea-LHCX1* combination is a remarkably effective quencher. If the model for green plant thylakoid membranes developed by Bennett et al (51)…”

Chloroplast ultrastructure in plants

“…For example, this approach reveals how the mesoscopic protein network of photosystem II (PSII) and LHCII complexes in stacked thylakoid grana domains establish ultrafast light harvesting (e.g. Amarnath et al ., ; Bennett et al ., ). The current restriction of cryo‐ET to visualize samples with a limited thickness prevents imaging of the chloroplast ultrastructure in intact plant tissues.…”

Quantitative modeling of energy dissipation in Arabidopsis thaliana

“…To make predictions of quenched fluorescence lifetimes observed in vivo, the quantum mechanical descriptions of energy transfer to quenching sites must be incorporated into larger energy transfer models. The multiscale model of energy transfer at the membrane scale discussed in Section 2.1 (Amarnath et al, 2016) has been developed to include quenching sites located at several of the suggested quenching sites in LHCII (Bennett et al, 2017) and can make predictions of fluorescence lifetimes given various quenching configurations. Changes in experimental fluorescence decay profiles of A. thaliana leaves (Sylak-Glassman et al, 2016) are accurately described by changes in a single effective quantity − the exciton diffusion length, L D .…”

“…The functional dependence can be thought of, in the simplest approximation, as product of the two quantitates. Although different combinations of the intrinsic quenching rate and density of quenching sites can describe the fluorescence snapshot data, they all have the same L D for a given quenched fluorescence lifetime (Bennett et al, 2017).…”

“…However, recent single molecule experiments on monomeric LHCIIs from pigment deficient mutants suggest that xanthophyll deficiencies instead change pigment-protein complex conformational dynamics, and therefore the activation of quenching sites (Tutkus et al, 2017). Integrating these data into coarse grained membrane scale models (Amarnath et al, 2016;Bennett et al, 2017) would be useful for evaluating the effects of xanthophyll deficiency on molecular mechanisms of quenching in addition to the regulation of quenching.…”