Abstract
Chloride ions can be translocated across cell membranes through Cl− channels or Cl−/H+ exchangers. The thylakoid-located member of the Cl− channel CLC family in Arabidopsis thaliana (AtCLCe) was hypothesized to play a role in photosynthetic regulation based on the initial photosynthetic characterization of clce mutant lines. The reduced nitrate content of Arabidopsis clce mutants suggested a role in regulation of plant nitrate homeostasis. In this study, we aimed to further investigate the role of AtCLCe in the regulation of ion homeostasis and photosynthetic processes in the thylakoid membrane. We report that the size and composition of proton motive force were mildly altered in two independent Arabidopsis clce mutant lines. Most pronounced effects in the clce mutants were observed on the photosynthetic electron transport of dark-adapted plants, based on the altered shape and associated parameters of the polyphasic OJIP kinetics of chlorophyll a fluorescence induction. Other alterations were found in the kinetics of state transition and in the macro-organization of photosystem II supercomplexes, as indicated by circular dichroism measurements. Pre-treatment with KCl but not with KNO3 restored the wild-type photosynthetic phenotype. Analyses by transmission electron microscopy revealed a bow-like arrangement of the thylakoid network and a large thylakoid-free stromal region in chloroplast sections from the dark-adapted clce plants. Based on these data, we propose that AtCLCe functions in Cl− homeostasis after transition from light to dark, which affects chloroplast ultrastructure and regulation of photosynthetic electron transport.
Highlights
Photosynthesis is essential for life on Earth
Cl− has been long considered to be the major counteranion during electron transport-coupled H+ translocation, whose import into the lumen is expected to result in rapid partial depolarization of the thylakoid membrane (Hind et al, 1974)
As the only anion channel so far localized to thylakoids, AtCLCe has been hypothesized to be responsible for the partial depolarization of the thylakoid membrane in the light (Finazzi et al, 2015; Pottosin and Dobrovinskaya, 2015)
Summary
Photosynthesis is essential for life on Earth. A key element of photosynthesis is conversion of sunlight energy into organic carbon via the generation of a membrane electrochemical potential gradient for protons (H+), known as the proton motive force (PMF). To generate PMF, pigments (chlorophylls and carotenoids) bound to proteins in light harvesting complexes (LHCs) absorb photons and transfer their excitation energy to the reaction centers of photosystems (PS). The excitation is converted into charge separation, which drives electron transport from PSII to PSI via the cytochrome b6f (Cyt b6f ) complex. The net result of this process is the oxidation of water molecules (oxygen evolution) and the reduction of NADP+, which is associated with translocation of H+ into the thylakoid lumen. A light-driven cyclic electron transport around PSI and Cyt b6f is operative, which does not evolve oxygen, nor induce
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