Reactive oxygen species (ROS)-dependent signaling pathways from chloroplasts and mitochondria merge at the nuclear protein RADICAL-INDUCED CELL DEATH1 (RCD1). RCD1 interacts in vivo and suppresses the activity of the transcription factors ANAC013 and ANAC017, which mediate a ROS-related retrograde signal originating from mitochondrial complex III. Inactivation of RCD1 leads to increased expression of mitochondrial dysfunction stimulon (MDS) genes regulated by ANAC013 and ANAC017. Accumulating MDS gene products, including alternative oxidases (AOXs), affect redox status of the chloroplasts, leading to changes in chloroplast ROS processing and increased protection of photosynthetic apparatus. ROS alter the abundance, thiol redox state and oligomerization of the RCD1 protein in vivo, providing feedback control on its function. RCD1-dependent regulation is linked to chloroplast signaling by 3'-phosphoadenosine 5'-phosphate (PAP). Thus, RCD1 integrates organellar signaling from chloroplasts and mitochondria to establish transcriptional control over the metabolic processes in both organelles.

Cyanobacteria and microalgae perform oxygenic photosynthesis where light energy is harnessed to split water into oxygen and protons. This process releases electrons that are used by the photosynthetic electron transport chain to form reducing equivalents that provide energy for the cell metabolism. Constant changes in environmental conditions, such as light availability, temperature, and access to nutrients, create the need to balance the photochemical reactions and the metabolic demands of the cell. Thus, cyanobacteria and microalgae evolved several auxiliary electron transport (AET) pathways to disperse the potentially harmful over‐supply of absorbed energy. AET pathways are comprised of electron sinks, e.g. flavodiiron proteins (FDPs) or other terminal oxidases, and pathways that recycle electrons around photosystem I, like NADPH‐dehydrogenase‐like complexes (NDH) or the ferredoxin‐plastoquinone reductase (FQR). Under controlled conditions the need for these AET pathways is decreased and AET can even be energetically wasteful. Therefore, redirecting photosynthetic reducing equivalents to biotechnologically useful reactions, catalyzed by i.e. innate hydrogenases or heterologous enzymes, offers novel possibilities to apply photosynthesis research.

Thioredoxins (TRXs) mediate light‐dependent activation of primary photosynthetic reactions in plant chloroplasts by reducing disulphide bridges in redox‐regulated enzymes. Of the two plastid TRX systems, the ferredoxin‐TRX system consists of ferredoxin‐thioredoxin reductase (FTR) and multiple TRXs, while the NADPH‐dependent thioredoxin reductase (NTRC) contains a complete TRX system in a single polypeptide. Using Arabidopsis plants overexpressing or lacking a functional NTRC, we have investigated the redundancy and interaction between the NTRC and Fd‐TRX systems in regulation of photosynthesis in vivo. Overexpression of NTRC raised the CO₂ fixation rate and lowered non‐photochemical quenching and acceptor side limitation of PSI in low light conditions by enhancing the activation of chloroplast ATP synthase and TRX‐regulated enzymes in Calvin–Benson cycle (CBC). Overexpression of NTRC with an inactivated NTR or TRX domain partly recovered the phenotype of knockout plants, suggesting crosstalk between the plastid TRX systems. NTRC interacted in planta with fructose‐1,6‐bisphosphatase, phosphoribulokinase and CF₁γ subunit of the ATP synthase and with several chloroplast TRXs. These findings indicate that NTRC‐mediated regulation of the CBC and ATP synthesis occurs both directly and through interaction with the ferredoxin‐TRX system and is crucial when availability of light is limiting photosynthesis.

Photosynthesis is a highly regulated process in photoautotrophic cells. The main goal of the regulation is to keep the basic photosynthetic reactions, i.e. capturing light energy, conversion into chemical energy and production of carbohydrates, in balance. The rationale behind the evolution of strong regulation mechanisms is to keep photosynthesis functional under all conditions encountered by sessile plants during their lifetimes. The regulatory mechanisms may, however, also impair photosynthetic efficiency by overriding the photosynthetic reactions in controlled environments like crop fields or bioreactors, where light energy could be used for production of sugars instead of dissipation as heat and down-regulation of carbon fixation. The plant chloroplast has a high number of regulatory proteins called thioredoxins (TRX), which control the function of chloroplasts from biogenesis and assembly of chloroplast machinery to light and carbon fixation reactions as well as photoprotective mechanisms. Here, we review the current knowledge of regulation of photosynthesis by chloroplast TRXs and assess the prospect of improving plant photosynthetic efficiency by modification of chloroplast thioredoxin systems.

Plants have adopted a number of mechanisms to restore redox homeostasis in the chloroplast under fluctuating light conditions in nature. Chloroplast thioredoxin systems are crucial components of this redox network, mediating environmental signals to chloroplast proteins. In the reduced state, thioredoxins control the structure and function of proteins by reducing disulfide bridges in the redox active site of a protein. Subsequently, an oxidized thioredoxin is reduced by a thioredoxin reductase, the two enzymes together forming a thioredoxin system. Plant chloroplasts have versatile thioredoxin systems, including two reductases dependent on ferredoxin and NADPH as reducing power, respectively, several types of thioredoxins, and the system to deliver thiol redox signals to the thylakoid membrane and lumen. Light controls the activity of chloroplast thioredoxin systems in two ways. First, light reactions activate the thioredoxin systems via donation of electrons to oxidized ferredoxin and NADP ⁺ , and second, light induces production of reactive oxygen species in chloroplasts which deactivate the components of the thiol redox network. The diversity and partial redundancy of chloroplast thioredoxin systems enable chloroplast metabolism to rapidly respond to ever-changing environmental conditions and to raise plant fitness in natural growth conditions.

Linear electron transport in the thylakoid membrane drives photosynthetic NADPH and ATP production, while cyclic electron flow (CEF) around photosystem I only promotes the translocation of protons from stroma to thylakoid lumen. The chloroplast NADH dehydrogenase‐like complex (NDH) participates in one CEF route transferring electrons from ferredoxin back to the plastoquinone pool with concomitant proton pumping to the lumen. CEF has been proposed to balance the ratio of ATP/NADPH production and to control the redox poise particularly in fluctuating light conditions, but the mechanisms regulating the NDH complex remain unknown. We have investigated potential regulation of the CEF pathways by the chloroplast NADPH‐thioredoxin reductase (NTRC) in vivo by using an Arabidopsis knockout line of NTRC as well as lines overexpressing NTRC. Here, we present biochemical and biophysical evidence showing that NTRC stimulates the activity of NDH‐dependent CEF and is involved in the regulation of generation of proton motive force, thylakoid conductivity to protons, and redox balance between the thylakoid electron transfer chain and the stroma during changes in light conditions. Furthermore, protein–protein interaction assays suggest a putative thioredoxin‐target site in close proximity to the ferredoxin‐binding domain of NDH, thus providing a plausible mechanism for redox regulation of the NDH ferredoxin:plastoquinone oxidoreductase activity.