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A Thylakoid-Located Two-Pore K+ Channel Controls Photosynthetic Light Utilization in Plants

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Science  04 Oct 2013:
Vol. 342, Issue 6154, pp. 114-118
DOI: 10.1126/science.1242113

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pH Gradient in Light of Electroneutrality

Photosynthesis in plant chloroplasts depends on a proton gradient to convert light energy into adenosine triphosphate. Studying Arabidopsis, Carraretto et al. (p. 114, published online 5 September; see the Perspective by Rochaix) identified the potassium channel TPK3 in the stacked membranes of the chloroplast's thylakoids as key to sustaining the proton gradient. As the thylakoid lumen acidifies on exposure to light, electroneutrality derives from TPK3 activity. TPK3 was able to optimize chloroplast responses to light across a wide range of intensities. Plants lacking functional TPK3 appeared normal when grown at modest light levels, but at higher light levels, the plants showed disruptions in overall growth and in thylakoid organization.

Abstract

The size of the light-induced proton motive force (pmf) across the thylakoid membrane of chloroplasts is regulated in response to environmental stimuli. Here, we describe a component of the thylakoid membrane, the two-pore potassium (K+) channel TPK3, which modulates the composition of the pmf through ion counterbalancing. Recombinant TPK3 exhibited potassium-selective channel activity sensitive to Ca2+ and H+. In Arabidopsis plants, the channel is found in the thylakoid stromal lamellae. Arabidopsis plants silenced for the TPK3 gene display reduced growth and altered thylakoid membrane organization. This phenotype reflects an impaired capacity to generate a normal pmf, which results in reduced CO2 assimilation and deficient nonphotochemical dissipation of excess absorbed light. Thus, the TPK3 channel manages the pmf necessary to convert photochemical energy into physiological functions.

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