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

Thioredoxins (TRX) play an important role in controlling photosynthetic acclimation to fluctuating light (FL), while the underlying mechanisms remain unclear. Here we used Arabidopsis mutants lacking NADPH-dependent TRX-reductase C (NTRC) or parts of the light-dependent TRX systems to investigate specific functions of this network in FL. In the wildtype, photosynthetic acclimation required three days to develop and stabilized after five days 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 due to a specifically 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, ntrc mutants showed an apparent lack of photoprotective responses that may explain their increased vulnerability under prolonged growth in FL. Results show that NADPH-dependent NTRC is balancing chloroplast redox-systems and Calvin-Benson-cycle activity during prolonged light variability, to optimize PSI, PSII and water-use efficiency, while having no direct effect on photoprotective mechanisms.