4.6 Article

Dissipation of the proton electrochemical gradient in chloroplasts promotes the oxidation of ATP synthase by thioredoxin-like proteins

Journal

JOURNAL OF BIOLOGICAL CHEMISTRY
Volume 298, Issue 11, Pages -

Publisher

ELSEVIER
DOI: 10.1016/j.jbc.2022.102541

Keywords

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Funding

  1. Japan Society for the Promotion of Science [21H02502]
  2. Dynamic Alliance for Open Innovation Bridging Human, Environment, and Materials [21H02502]
  3. [22J13334]

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This study demonstrates that the redox regulation of CFoCF1 in ATP synthesis under light conditions is influenced by the oxidation of CF1-γ subunit and physiological oxidants in the chloroplast. The generation status of Delta mu H+ controls the redox regulation of CFoCF1 to prevent energetic disadvantages in plants.
Chloroplast FoF1-ATP synthase (CFoCF1) uses an electro-chemical gradient of protons across the thylakoid membrane (Delta mu H+) as an energy source in the ATP synthesis reaction. CFoCF1 activity is regulated by the redox state of a Cys pair on its central axis, that is, the gamma subunit (CF1-gamma). When the Delta mu H+ is formed by the photosynthetic electron transfer chain under light conditions, CF1-gamma is reduced by thioredoxin (Trx), and the entire CFoCF1 enzyme is activated. The redox regulation of CFoCF1 is a key mechanism underlying the control of ATP synthesis under light conditions. In contrast, the oxidative deactivation process involving CFoCF1 has not been clarified. In the present study, we analyzed the oxidation of CF1-gamma by two physiological oxidants in the chloroplast, namely the proteins Trx-like 2 and atypical Cys-His-rich Trx. Using the thylakoid membrane containing the reduced form of CFoCF1, we were able to assess the CF1-gamma oxidation ability of these Trx-like proteins. Our kinetic analysis indicated that these proteins oxidized CF1-gamma with a higher efficiency than that achieved by a chemical oxidant and typical chloroplast Trxs. Additionally, the CF1-gamma oxidation rate due to Trx-like proteins and the af-finity between them were changed markedly when Delta mu H+ for-mation across the thylakoid membrane was manipulated artificially. Collectively, these results indicate that the forma-tion status of the Delta mu H+ controls the redox regulation of CFoCF1 to prevent energetic disadvantages in plants.

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