Dissection of photosynthetic short- and long-term acclimation to fluctuating light reveals specific functions of the chloroplast thioredoxin network

Thioredoxins (TRXs) play an important role in controlling photosynthetic acclimation to fluctuating light (FL), but the underlying mechanisms remain unclear. Here, we used Arabidopsis mutants lacking NADPH-dependent TRX-reductase C (NTRC) or parts of the light-dependent TRX system to investigate the specific functions of this network in FL. In the wild type, photosynthetic acclimation required 3 d to develop and stabilized after 5 d of growth in FL. In the ntrc mutant, these acclimation responses were strongly attenuated, leading to decreased PSII acceptor availability, increased non-photochemical quenching (NPQ), and impaired PSII quantum efficiency. Moreover, PSI performance decreased, while acceptor-side limitation of PSI increased. This was particularly due to a strong decline in the reduction states of 2-Cys-peroxiredoxins and fructose-1,6-bisphosphatase, resulting in decreased CO2-fixation rates and delayed relaxation of NPQ in the low-light phases of FL. Since this was not reflected by changes in de-epoxidation of violaxanthin, state transition, or chlorophyll a level, the ntrc mutants showed an apparent lack of photoprotective responses that might explain their increased vulnerability under prolonged growth in FL. Our results show that NADPH-dependent NTRC balances chloroplast redox-systems to optimize the activity of the Calvin-Benson cycle during prolonged light variability in order to optimize PSI, PSII, and water-use efficiency, while having no direct effect on photoprotective mechanisms.