Complex Roles of PsbS and Xanthophylls in the Regulation of Nonphotochemical Quenching in Arabidopsis thaliana under Fluctuating Light

Abstract

Protection of photosystem II against damage from excess light by nonphotochemical quenching (NPQ) includes responses on a wide range of timescales. The onset of the various phases of NPQ overlap in time making it difficult to discern if they influence each other or involve different photophysical mechanisms. To unravel the complex relationship of the known actors in NPQ, we perform fluorescence lifetime snapshot measurements throughout multiple cycles of alternating 2 min periods of high light and darkness. By comparing the data with an empirically based mathematical model that describes both fast and slow quenching responses, we suggest that the rapidly reversible quenching response depends on the state of the slower response. By studying a series of Arabidopsis thaliana mutants, we find that removing zeaxanthin (Zea) or enhancing PsbS concentration, for example, influences the amplitudes of the slow quenching induction and recovery, but not the timescales. The plants' immediate response to high light appears independent of the illumination history, while PsbS and Zea have distinct roles in both quenching and recovery. We further identify two parameters in our model that predominately influence the recovery amplitude and propose that our approach may prove useful for screening new mutants or overexpressors with enhanced biomass yields under field conditions.

Mechanisms shaping the synergism of zeaxanthin and PsbS in photoprotective energy dissipation in the photosynthetic apparatus of plants

“…Figure 1B presents light intensity profiles of NPQ determined for A. thaliana WT as well as for the npq1 and npq4 mutants. As can be seen, the simultaneous presence of both Zea and PsbS protein is necessary for the photosynthetic apparatus to develop a significantly high photoprotective response, in accordance with the previous reports (Niyogi et al, 1998;Li et al, 2000;Steen et al, 2020). The levels of NPQ determined for different genotypes of A. thaliana in the present work are in agreement with the reported values corresponding to comparable light intensities (Kress and Jahns, 2017).…”

“…It has been demonstrated that the most effective excitation quenching requires the simultaneous presence of both the PsbS protein (Li et al, 2000) and zeaxanthin (Zea) (Niyogi et al, 1998), a xanthophyll accumulated under high light conditions in consequence of de-epoxidation of violaxanthin (Vio) within the xanthophyll cycle (Jahns et al, 2009) (see Supplemental Figure 1). Moreover, overexpression of PsbS in plants results in enhanced light-induced excitation quenching (Steen et al, 2020). The significant quenching of Chl a excitations has been observed in reconstituted LHCII with the presence of Zea and PsbS, although neither PsbS nor Zea alone was sufficient to induce the same effect (Wilk et al, 2013).…”

Light Quality-Dependent Regulation of Non-Photochemical Quenching in Tomato Plants

“…The initial step of photosynthesis involves the absorption of light. However, when the amount of light absorbed exceeds the capacity of its photosynthetic utilization, this can lead to the formation of reactive oxygen species (ROS) and damage to the photosynthetic apparatus [ 1 , 2 ]. To reduce the risk of potential damage plants evolved protective mechanisms, including ways to minimize light absorption, detoxify ROS and dissipate excess light energy as heat [ 3 ].…”

An energy-dissipative state of the major antenna complex of plants

“…Method used is adapted for fluorescence lifetime snapshot from (59) and transient absorption spectroscopy snapshot from (60). For fluorescence lifetime measurements, time-correlated single photon counting (TCSPC) was performed on detached leaves, isolated thylakoids and gel filtration fractions.…”