H+ Transport by K+ EXCHANGE ANTIPORTER3 Promotes Photosynthesis and Growth in Chloroplast ATP Synthase Mutants.

Viviana Correa Galvis,Beata Siemiatkowska,Rainer Höfgen,Deserah D Strand,Franziska Brückner,Stephanie Bethmann,Michal Uflewski,Bethan A Morris,Michaela Messer,Ute Armbruster,Szilvia Z Tóth,Peter Jahns,Wolfram Thiele,Dennis Hübner,Mark Aurel Schöttler,Mutsumi Watanabe,Elias Kaiser

doi:10.1104/pp.19.01561

Abstract

The composition of the thylakoid proton motive force (pmf) is regulated by thylakoid ion transport. Passive ion channels in the thylakoid membrane dissipate the membrane potential (Δψ) component to allow for a higher fraction of pmf stored as a proton concentration gradient (ΔpH). K+/H+ antiport across the thylakoid membrane via K+ EXCHANGE ANTIPORTER3 (KEA3) instead reduces the ΔpH fraction of the pmf. Thereby, KEA3 decreases nonphotochemical quenching (NPQ), thus allowing for higher light use efficiency, which is particularly important during transitions from high to low light. Here, we show that in the background of the Arabidopsis (Arabidopsis thaliana) chloroplast (cp)ATP synthase assembly mutant cgl160, with decreased cpATP synthase activity and increased pmf amplitude, KEA3 plays an important role for photosynthesis and plant growth under steady-state conditions. By comparing cgl160 single with cgl160 kea3 double mutants, we demonstrate that in the cgl160 background loss of KEA3 causes a strong growth penalty. This is due to a reduced photosynthetic capacity of cgl160 kea3 mutants, as these plants have a lower lumenal pH than cgl160 mutants, and thus show substantially increased pH-dependent NPQ and decreased electron transport through the cytochrome b 6 f complex. Overexpression of KEA3 in the cgl160 background reduces pH-dependent NPQ and increases photosystem II efficiency. Taken together, our data provide evidence that under conditions where cpATP synthase activity is low, a KEA3-dependent reduction of ΔpH benefits photosynthesis and growth.

Highlights

IntroductionK1 EXCHANGE ANTIPORTER3 (KEA3) Upregulates Photosynthesis in cgl160 Mutants (Li et al, 2004; Correa-Galvis et al, 2016; Sacharz et al, 2017)
To obtain information about the stoichiometric relationship of the proton-transporting mechanisms mediated by the cpATP synthase and K1 EXCHANGE ANTIPORTER3 (KEA3), we titrated thylakoid membranes from the wild type against heterologously expressed and purified KEA3 soluble C terminus and ATP synthase CFo subunit b (AtpF) with
From the quantifications obtained by protein blot analyses, we calculated an average abundance in thylakoid membranes of about 4.15 mmol/mol chlorophyll (Chl) for KEA3 (Fig. 1B), and 413 mmol/mol Chl for AtpF (Fig. 1C)

Summary

Introduction

KEA3 Upregulates Photosynthesis in cgl160 Mutants (Li et al, 2004; Correa-Galvis et al, 2016; Sacharz et al, 2017) This so-called energy-dependent quenching (qE) component of nonphotochemical quenching (NPQ) is further sustained by zeaxanthin production via the low pH-activated violaxanthin de-epoxidase (VDE) localized in the lumen of land plants (Hager, 1969; Niyogi et al, 1998). The same has been reported for tobacco (Nicotiana benthamiana) and Arabidopsis (Arabidopsis thaliana) mutants with constitutively lower cpATP synthase conductivity, due to decreased levels or activities, which have high pmf and a large fraction of it stored as DC (Rott et al, 2011; Fristedt et al, 2015; Davis et al., 2016) Whether and how this adjusted pmf composition affects photosynthesis and growth remains to be determined

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