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Intertwined translational regulations set uneven stoichiometry of chloroplast ATP synthase subunits.

ABSTRACT: The (C)F1 sector from H(+)-ATP synthases comprises five subunits: alpha, beta, gamma, delta and epsilon, assembled in a 3:3:1:1:1 stoichiometry. Here, we describe the molecular mechanism ensuring this unique stoichiometry, required for the functional assembly of the chloroplast enzyme. It relies on a translational feedback loop operating in two steps along the assembly pathway of CF1. In Chlamydomonas, production of the nucleus-encoded subunit gamma is required for sustained translation of the chloroplast-encoded subunit beta, which in turn stimulates the expression of the chloroplast-encoded subunit alpha. Translational downregulation of subunits beta or alpha, when not assembled, is born by the 5'UTRs of their own mRNAs, pointing to a regulation of translation initiation. We show that subunit gamma, by assembling with alpha(3)beta(3) hexamers, releases a negative feedback exerted by alpha/beta assembly intermediates on translation of subunit beta. Moreover, translation of subunit alpha is transactivated by subunit beta, an observation unprecedented in the biogenesis of organelle proteins.

SUBMITTER: Drapier D

PROVIDER: S-EPMC1948998 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The chloroplast ATP synthase catalyzes the light-driven synthesis of ATP and is activated in the light and inactivated in the dark by redox-modulation through the thioredoxin system. It has been proposed that this down-regulation is important for preventing wasteful hydrolysis of ATP in the dark. To test this proposal, we compared the effects of extended dark exposure in Arabidopsis lines expressing the wild-type and mutant forms of ATP synthase that are redox regulated or constitutively active. In contrast to the predictions of the model, we observed that plants with wild-type redox regulation lost photosynthetic capacity rapidly in darkness, whereas those expressing redox-insensitive form were far more stable. To explain these results, we propose that in wild-type plants, down-regulation of ATP synthase inhibits ATP hydrolysis, leading to dissipation of thylakoid proton motive force (pmf) and subsequent inhibition of protein transport across the thylakoid through the twin arginine transporter (Tat)-dependent and Sec-dependent import pathways, resulting in the selective loss of specific protein complexes. By contrast, in mutants with a redox-insensitive ATP synthase, pmf is maintained by ATP hydrolysis, thus allowing protein transport to maintain photosynthetic activities for extended periods in the dark. Hence, a basal level of Tat-dependent, as well as, Sec-dependent import activity, in the dark helps replenishes certain components of the photosynthetic complexes and thereby aids in maintaining overall complex activity. However, the influence of a dark pmf on thylakoid protein import, by itself, could not explain all the effects we observed in this study. For example, we also observed in wild type plants a large transient buildup of thylakoid pmf and nonphotochemical exciton quenching upon sudden illumination of dark adapted plants. Therefore, we conclude that down-regulation of the ATP synthase is probably not related to preventing loss of ATP per se. Instead, ATP synthase redox regulation may be impacting a number of cellular processes such as (1) the accumulation of chloroplast proteins and/or ions or (2) the responses of photosynthesis to rapid changes in light intensity. A model highlighting the complex interplay between ATP synthase regulation and pmf in maintaining various chloroplast functions in the dark is presented. Significance Statement: We uncover an unexpected role for thioredoxin modulation of the chloroplast ATP synthase in regulating the dark-stability of the photosynthetic apparatus, most likely by controlling thylakoid membrane transport of proteins and ions.

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Intertwined translational regulations set uneven stoichiometry of chloroplast ATP synthase subunits.

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