Two different thiol redox systems exist in plant chloroplasts, the ferredoxin-thioredoxin (Trx) system, which depends on ferredoxin reduced by the photosynthetic electron transport chain and, thus, on light, and the NADPH-dependent Trx reductase C (NTRC) system, which relies on NADPH and thus may be linked to sugar metabolism in the dark. Previous studies suggested, therefore, that the two different systems may have different functions in plants. We now report that there is a previously unrecognized functional redundancy of Trx f1 and NTRC in regulating photosynthetic metabolism and growth. In Arabidopsis (Arabidopsis thaliana) mutants, combined, but not single, deficiencies of Trx f1 and NTRC led to severe growth inhibition and perturbed light acclimation, accompanied by strong impairments of Calvin-Benson cycle activity and starch accumulation. Light activation of key enzymes of these pathways, fructose-1,6-bisphosphatase and ADP-glucose pyrophosphorylase, was almost completely abolished. The subsequent increase in NADPH-NADP + and ATP-ADP ratios led to increased nitrogen assimilation, NADP-malate dehydrogenase activation, and light vulnerability of photosystem I core proteins. In an additional approach, reporter studies show that Trx f1 and NTRC proteins are both colocalized in the same chloroplast substructure. Results provide genetic evidence that light-and NADPH-dependent thiol redox systems interact at the level of Trx f1 and NTRC to coordinately participate in the regulation of the Calvin-Benson cycle, starch metabolism, and growth in response to varying light conditions. Reversible disulfide bond formation between two Cys residues regulates structure and function of many proteins in diverse organisms (Cook and Hogg, 2013). Thiol disulfide exchange is controlled by thioredoxins (Trxs), which are small proteins containing a redoxactive disulfide group in their active site (Holmgren, 1985;Baumann and Juttner, 2002). The latter can be reduced to a dithiol by Trx reductases using NADPH or ferredoxin (Fdx) as electron donors. Due to their low redox midpoint potential, reduced Trxs are able to reductively cleave disulfide bonds in many target proteins and, thus, modulate their functions.Plants contain the most versatile Trx system found in all organisms with respect to the multiplicity of different isoforms and reduction systems (Buchanan and Balmer, 2005;Nikkanen and Rintamäki, 2014;Geigenberger and Fernie, 2014). The Arabidopsis (Arabidopsis thaliana) genome contains a complex family of Trxs, including up to 20 different isoforms grouped into seven subfamilies (Schürmann and Buchanan, 2008;Dietz and Pfannschmidt, 2011). Trxs f1-2, m1-4, x, y1-2, and z are located exclusively in the chloroplast, and Trx o is located exclusively in the mitochondria, while the eight Trx h representatives are distributed between the cytosol, nucleus, endoplasmic reticulum, and mitochondria (Meyer et al., 2012). The different Trxs can be reduced by two different redox systems, dependent on Fdx and Fdx-Trx reductase in the chlorop...

Sunlight represents the energy source for photosynthesis and plant growth. When growing in the field, plant photosynthesis has to manage strong fluctuations in light intensities. Regulation based on the thioredoxin (Trx) system is believed to ensure light-responsive control of photosynthetic reactions in the chloroplast. However, direct evidence for a role of this system in regulating dynamic acclimation of photosynthesis in fluctuating conditions is largely lacking. In this report we show that the ferredoxin-dependent Trxs m1 and m2 as well as the NADPH-dependent NTRC are both indispensable for photosynthetic acclimation in fluctuating light intensities. Arabidopsis mutants with combined deficiency in Trxs m1 and m2 show wild-type growth and photosynthesis under constant light condition, while photosynthetic parameters are strongly modified in rapidly alternating high and low light. Two independent trxm1m2 mutants show lower photosynthetic efficiency in high light, but surprisingly significantly higher photosynthetic efficiency in low light. Our data suggest that a main target of Trx m1 and m2 is the NADP-malate dehydrogenase involved in export of excess reductive power from the chloroplast. The decreased photosynthetic efficiency in the high-light peaks may thus be explained by a reduced capacity of the trxm1m2 mutants in the rapid light activation of this enzyme. In the ntrc mutant, dynamic responses of non-photochemical quenching of excitation energy and plastoquinone reduction state both were strongly attenuated in fluctuating light intensities, leading to a massive decrease in PSII quantum efficiency and a specific decrease in plant growth under these conditions. This is likely due to the decreased ability of the ntrc mutant to control the stromal NADP(H) redox poise. Taken together, our results indicate that NTRC is indispensable in ensuring the full range of dynamic responses of photosynthesis to optimize photosynthesis and maintain growth in fluctuating light, while Trxs m1 and m2 are indispensable for full activation of photosynthesis in the high-light periods but negatively affect photosynthetic efficiency in the low-light periods of fluctuating light.