The impact of light and thioredoxins on the plant thiol-disulfide proteome

Abstract

Thiol-based redox regulation is a crucial post-translational mechanism to acclimate plants to changing light availability. Here, we conduct a biotin-switch-based redox proteomics study to systematically investigate dynamics of the thiol-redox network in response to temporal changes in light availability and across genotypes lacking parts of the thioredoxin (Trx) or NADPH-Trx-reductase C (NTRC) systems in the chloroplast. Time-resolved dynamics revealed light leading to marked decreases in the oxidation states of many chloroplast proteins with photosynthetic functions during the first 10 min, followed by their partial re-oxidation after 2-6 hours into the photoperiod. This involved f, m and x-type Trx proteins showing similar light-induced reduction-oxidation dynamics, while NTRC, 2-Cys-Prx and Trx y2 showed an opposing pattern, being more oxidized in the light than the dark. In Arabidopsis trxf1f2, trxm1m2 or ntrc mutants, in the light most proteins showed increased oxidation states than wild type, suggesting their light-dependent dynamics being related to the NTRC/Trx networks. While NTRC deficiency had a strong influence in all light conditions, deficiencies in f- or m-type Trxs showed differential impacts on the thiol-redox proteome depending on the light environment, being higher in constant or fluctuating light, respectively. Results indicate plant redox proteomes to be subject to dynamic changes in reductive and oxidative pathways to cooperatively fine-tune photosynthetic and metabolic processes in the light. This involves f-type Trxs and NTRC to play a role in constant medium light, while both m-type Trxs and NTRC being important to balance changes in protein redox-pattern during dynamic alterations in fluctuating light intensities. One sentence summaryThe plant protein redoxome shows light-dependent reduction and reoxidation dynamics linked to Trxs f1/f2, m1/m2 and NTRC, being of different importance depending on the extent of light variability.