Regulation and Levels of the Thylakoid K⁺/H⁺Antiporter KEA3 Shape the Dynamic Response of Photosynthesis in Fluctuating Light

Abstract

Crop canopies create environments of highly fluctuating light intensities. In such environments, photoprotective mechanisms and their relaxation kinetics have been hypothesized to limit photosynthetic efficiency and therefore crop yield potential. Here, we show that overexpression of the Arabidopsis thylakoid K+/H+ antiporter KEA3 accelerates the relaxation of photoprotective energy-dependent quenching after transitions from high to low light in Arabidopsis and tobacco. This, in turn, enhances PSII quantum efficiency in both organisms, supporting that in wild-type plants, residual light energy quenching following a high to low light transition represents a limitation to photosynthetic efficiency in fluctuating light. This finding underscores the potential of accelerating quenching relaxation as a building block for improving photosynthetic efficiency in the field. Additionally, by overexpressing natural KEA3 variants with modification to the C-terminus, we show that KEA3 activity is regulated by a mechanism involving its lumen-localized C-terminus, which lowers KEA3 activity in high light. This regulatory mechanism fine-tunes the balance between photoprotective energy dissipation in high light and maximum quantum yield in low light, likely to be critical for efficient photosynthesis in fluctuating light conditions.

Fluctuating light experiments and semi-automated plant phenotyping enabled by self-built growth racks and simple upgrades to the IMAGING-PAM

“…Under constant light, only kea3 showed slightly elevated NPQ compared to WT ( Figure 6K, M). This matches earlier results at similar light intensities (Armbruster et al, 2016). NPQ for stn7 mutants showed slightly depressed NPQ compared to WT whereas steady-state NPQ in vccn1 mostly behaved like the wild-type control ( Figure 6K, M), confirming recent results (Duan et al, 2016;Herdean et al, 2016).…”

Maintenance of pre‐existing DNA methylation states through recurring excess‐light stress

“…How the interplay of the three xanthophyll cycle pigments in the primed state are influencing the kinetics of NPQ, or the extent to which this was driven by proton motive force and ΔpH, remains to be resolved and would be of interest for further investigation (Armbruster, Correa Galvis, Kunz, & Strand, 2017). Regardless of the mechanism, it is clear that the plants have been primed to react differently to light stress, inducing a faster induction and relaxation, which is an agronomically important trait (Armbruster et al, 2014(Armbruster et al, , 2016.…”

Fine‐tuned regulation of the K+/H+ antiporter KEA3 is required to optimize photosynthesis during induction

“…We propose a model in which the N-terminal end is facing to the lumen whereas the C-terminal KTN domain is exposed to the stroma (Figure 4b). During the preparation of this manuscript, a different topology model of KEA3, in which the KTN domain was localized to the luminal side, was proposed on the basis of the results of a thermolysin protection assay of a GFP-tagged KEA3 (Armbruster et al, 2016). Despite the opposite membrane topology, the same orientation of H + / K + movement was proposed in their work.…”