SignificanceChloroplasts harbor a complex redox network formed by two systems, the FTR- thioredoxins (Trxs), which relies on photoreduced ferredoxin (Fd), and the NADPH-dependent Trx reductase C NTRC. Thus, an important issue in chloroplast biology is to establish the relationship between these redox pathways. Here we propose that the Fd-FTR-Trxs and NTRC redox systems are integrated via the redox balance of 2-Cys peroxiredoxins (Prxs), which therefore has a key role in chloroplast function. NTRC controls the redox balance of 2-Cys Prxs, which maintains the reducing capacity of the pool of chloroplast Trxs and, consequently, proper regulation of photosynthetic carbon assimilation enzymes. Therefore, redox regulation of chloroplast enzymes and hydrogen peroxide reduction are linked by the action of the NTRC-2-Cys Prxs system.

Light is probably the most important environmental stimulus for plant development. As sessile organisms, plants have developed regulatory mechanisms that allow the rapid adaptation of their metabolism to changes in light availability. Redox regulation based on disulfide-dithiol exchange constitutes a rapid and reversible post-translational modification, which affects protein conformation and activity. This regulatory mechanism was initially discovered in chloroplasts when it was identified that enzymes of the Calvin-Benson cycle (CBC) are reduced and active during the day and become rapidly inactivated by oxidation in the dark. At present, the large number of redox-sensitive proteins identified in chloroplasts extend redox regulation far beyond the CBC. The classic pathway of redox regulation in chloroplasts establishes that ferredoxin (Fdx) reduced by the photosynthetic electron transport chain fuels reducing equivalents to the large set of thioredoxins (Trxs) of this organelle via the activity of a Fdx-dependent Trx reductase (FTR), hence linking redox regulation to light. In addition, chloroplasts harbor an NADPH-dependent Trx reductase with a joint Trx domain, termed NTRC. The presence in chloroplasts of this NADPH-dependent redox system raises the question of the functional relationship between NTRC and the Fdx-FTR-Trx pathways. Here, we update the current knowledge of these two redox systems focusing on recent evidence showing their functional interrelationship through the action of the thiol-dependent peroxidase, 2-Cys peroxiredoxin (2-Cys Prx). The relevant role of 2-Cys Prxs in chloroplast redox homeostasis suggests that hydrogen peroxide may exert a key function to control the redox state of stromal enzymes. Indeed, recent reports have shown the participation of 2-Cys Prxs in enzyme oxidation in the dark, thus providing an explanation for the long-lasting question of photosynthesis deactivation during the light-dark transition.