Evolution and regulatory diversification of plastid F1FO-ATP synthase

F1FO-ATP synthase, the enzyme complex responsible for adenosine triphosphate (ATP) production, is universally conserved and central to cellular energy metabolism in bacteria as well as in mitochondria and plastids-organelles derived from ancestral bacteria. Although its basic structure and rotational catalytic mechanism are conserved, F1FO-ATP synthase exhibits remarkable regulatory diversity, which is evident in its structural variations, tissue-specific isoforms, and ATP synthesis and hydrolysis mechanisms, reflecting the metabolic demands and environmental contexts of different organisms and organelles. Among the diverse F1FO-ATP synthase isoforms, the plastid F1FO-ATP synthase exhibits unique regulatory features, including redox-dependent modulation, which adjusts enzyme activity in response to light availability. Certain angiosperms possess two isoforms of the γ subunit, encoded by ATPC1 and ATPC2, which give rise to redox-sensitive and redox-insensitive forms of the enzyme, respectively. The latter is active in the dark and may contribute to the maintenance of the proton motive force regulation, thereby supporting stress adaptation in non-photosynthetic tissues. In this review, through a phylogenetic analysis of the γ subunit, we integrate structural, physiological, and evolutionary aspects of plastid F1FO-ATP synthase and discuss how the diversification of ATP synthases, especially within plastid, underpins their broader physiological significance beyond ATP production. Furthermore, we discuss why the chloroplast ATP synthase must be redox-regulated.