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Plant Physiol. 2019 May 3. pii: pp.00255.2019. doi: 10.1104/pp.19.00255. [Epub ahead of print]

Photosynthesis in Arabidopsis thaliana is unaffected by the function of the vacuolar K+ channel TPK3.

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Washington State University CITY: Pullman STATE: Washington United States Of America [US].
Max Planck Institute of Molecular Plant Physiology CITY: Golm (Potsdam) Germany [DE].
Max Planck Institute for Molecular Plant Physiology CITY: Potsdam Germany [DE].
Washington State University CITY: Pullman STATE: WA United States Of America [US].
Washington State University CITY: Pullman STATE: WA POSTAL_CODE: 67659 United States Of America [US].
LMU Muenchen CITY: Martinsried Germany [DE].
LMU Muenchen CITY: Martinsried POSTAL_CODE: 82152 Germany [DE].
Michigan State University CITY: East Lansing STATE: Michigan POSTAL_CODE: 48824-1312 United States Of America [US].
Max Planck Institute of Molecular Plant Physiology CITY: Golm (Potsdam) POSTAL_CODE: 14476 Germany [DE].
Washington State University CITY: Pullman STATE: WA POSTAL_CODE: 99164-4236 United States Of America [US]


Photosynthesis is limited by the slow relaxation of non-photochemical quenching, which primarily dissipates excess absorbed light energy as heat. Because the heat dissipation process is proportional to light-driven thylakoid lumen acidification, manipulating thylakoid ion and proton flux via transport proteins could improve photosynthesis. However, an important aspect of our current understanding of the thylakoid ion transportome is inaccurate. Using fluorescent protein fusions, we show that the Arabidopsis thaliana two-pore K+ channel TPK3, which had been reported to mediate thylakoid K+ flux, localizes to the tonoplast not the thylakoid. The localization of TPK3 outside of the thylakoids is further supported by the absence of TPK3 in isolated thylakoids as well as the inability of isolated chloroplasts to import TPK3 protein. In line with the subcellular localization of TPK3 in the vacuole, we observed that photosynthesis in the Arabidopsis null mutant tpk3-1, which carries a T-DNA insertion in the first exon, remains unaffected. To gain a comprehensive understanding of how thylakoid ion flux impacts photosynthetic efficiency under dynamic growth light regimes, we performed long-term photosynthesis imaging of established and newly isolated trans-thylakoid K+- and Cl--flux mutants. Our results underpin the importance of thylakoid ion transport proteins potassium cation efflux antiporter KEA3 and voltage-dependent chloride channel VCCN1 and suggest that the activity of yet unknown K+ channel(s), but not TPK3, is critical for optimal photosynthesis in dynamic light environments.

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