Thiamine triphosphate puts the brake on the activation state of chloroplast ATP synthase.

Abstract

Metabolic effectors are critical in orchestrating biological processes. B vitamin-derived coenzymes are vital for coordinating metabolic enzyme activities, the disruption of which has been linked to numerous diseases in humans and fitness in plants. Modified derivatives of these coenzymes exist and could act as effectors to regulate certain metabolic processes but remain unexplored. Here, we demonstrate that the non-coenzyme vitamin B1 derivative thiamine triphosphate is transiently produced early during the light period in Arabidopsis thaliana (Arabidopsis). The production of this compound is driven by a chemiosmotic mechanism in the chloroplast, which contrasts with mammalian neuronal cells, where it is produced in the mitochondria. Using biophysical techniques of photosynthesis, we show that thiamine triphosphate serves to brake the activation state of chloroplast ATP synthase. This effect is suggested to be achieved by the opportune biosynthesis of thiamine triphosphate from inorganic phosphate and the coenzyme thiamine diphosphate in chloroplasts, which alters the substrate budget of photosynthesis, affecting the coordination of ATP synthesis and consumption during the Calvin-Benson cycle. Intriguingly, the absence of thiamine triphosphate alters the expression of plastid-encoded ATP synthase subunits. The study expands our knowledge on coenzyme derivatives as regulatory molecules in biological systems and, in this case, their regulation of energy metabolism.