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

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 (<i>Arabidopsis thaliana</i>) chloroplast (cp)ATP synthase assembly mutant <i>cgl160</i>, 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 <i>cgl160</i> single with <i>cgl160 kea3</i> double mutants, we demonstrate that in the <i>cgl160</i> background loss of KEA3 causes a strong growth penalty. This is due to a reduced photosynthetic capacity of <i>cgl160 kea3</i> mutants, as these plants have a lower lumenal pH than <i>cgl160</i> mutants, and thus show substantially increased pH-dependent NPQ and decreased electron transport through the cytochrome <i>b</i> _<i>6</i> <i>f</i> complex. Overexpression of <i>KEA3</i> in the <i>cgl160</i> 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.