Modification of Activity of the Thylakoid H⁺/K⁺ Antiporter KEA3 Disturbs ∆pH-Dependent Regulation of Photosynthesis

Abstract

The thylakoid K 1 efflux antiporter 3 (KEA3) is required for regulating components of the proton motive force (pmf), proton concentration gradient (DpH), and membrane potential (Dc). The Arabidopsis (Arabidopsis thaliana) disturbed proton gradient regulation mutant (dpgr) is a dominant allele of KEA3, conferring disturbed transport activity. Here, we show that overexpressing the DPGR-type KEA3 (DPGRox) retarded plant growth, whereas overexpressing the wild-type KEA3 (KEA3ox) did not. In KEA3ox lines, the contribution of Dc to pmf was enhanced, but in DPGRox lines, the size of pmf was reduced. In DPGRox plants, proton conductivity of the thylakoid membrane (g H 1) was elevated under high light, implying disturbed stoichiometry of H 1 /K 1 antiport through DPGR-type KEA3 rather than simply enhanced activity. The DpHdependent regulation consisting of thermal dissipation of excessively absorbed light energy and downregulation of cytochrome b 6 f complex activity was severely and mildly affected in DPGRox and KEA3ox plants, respectively. Consequently, photosystem I was sensitive to fluctuating light in both transgenic plants. Both photosystems were sensitive to constant high light and were slightly photodamaged even at standard growth light intensity in DPGRox plants. KEA3 regulates the components of pmf and optimizes the operation of ΔpH-dependent regulation of electron transport.

Collaboration between NDH and KEA3 Allows Maximally Efficient Photosynthesis after a Long Dark Adaptation

“…5). This is consistent with the fact that the contribution of KEA3 is not observed at high light intensities (Wang and Shikanai, 2019). The second phase is probably specifically observed at a relatively low light intensity, at which the transiently induced ∆pH-dependent downregulation is relaxed.…”

Phylogenetic Diversity and Physiological Roles of Plant Monovalent Cation/H+ Antiporters

“…A dominant mutant allele of KEA3, disturbed proton gradient regulation (dpgr) , showed reduced non-photochemical energy quenching (NPQ) during induction of photosynthesis ( Wang et al., 2017 ). Overexpressing the DPGR-type KEA3 (DPGRox) inhibited plant growth, with disturbed ΔpH-dependent regulation of electron transport ( Wang and Shikanai, 2019 ). It was recently shown that AtKEA3 benefited photosynthesis and growth in chloroplast ATP synthase-compromised mutant, via a KEA3-dependent reduction of ΔpH ( Correa Galvis et al., 2020 ).…”

Inactivation of mitochondrial Complex I stimulates chloroplast ATPase in Physcomitrella (Physcomitrium patens)

“…It is interesting to point out that this difference emerged as a consequence of the illumination since it became detectable only if plants were exposed to light for more than 120 seconds (Figure 6B and Figure S7). This suggests that the alterations in pmf partitioning emerged as a result of modifications in the photosynthetic activity (Avenson et al, 2005; Wang and Shikanai, 2019). This difference between genotypes was again light intensity-dependent and using a stronger, fully saturating, illumination (1000 μmol photons m -2 s -1 ) mutants were indistinguishable from WT (Figure S8).…”