Plant NADPH-dependent thioredoxin reductases are crucial for the metabolism of sink leaves and plant acclimation to elevated CO2

Plants contain three NADPH-thioredoxin reductases (NTR) located in the cytosol/mitochondria (NTRA/B) and the plastid (NTRC) with important metabolic functions. However, mutants deficient in all NTRs remained to be investigated. Here, we generated and characterised the triple Arabidopsis ntrabc mutant alongside with ntrc single and ntrab double mutants under different environmental conditions. Both ntrc and ntrabc mutants showed reduced growth and substantial metabolic alterations, especially in sink leaves and under high CO2 (HC), as compared to the wild type. However, ntrabc showed higher effective quantum yield of PSII under both constant and fluctuating light conditions, altered redox states of NADH/NAD(+) and glutathione (GSH/GSSG) and lower potential quantum yield of PSII in sink leaves in ambient but not high CO2 concentrations, as compared to ntrc, suggesting a functional interaction between chloroplastic and extra-chloroplastic NTRs in photosynthesis regulation depending on leaf development and environmental conditions. Our results unveil a previously unknown role of the NTR system in regulating sink leaf metabolism and plant acclimation to HC, while it is not affecting full plant development, indicating that the lack of the NTR system can be compensated, at least to some extent, by other redox mechanisms.

Automated summary

Plants have a NADPH-thioredoxin reductase (NTR) system consisting of three enzymes located in different cellular compartments with important metabolic functions. In this study, the effects of NTR deficiency were investigated using Arabidopsis mutants. The results showed that NTR deficiency led to reduced growth and metabolic alterations in sink leaves, especially under high CO2 conditions. Interestingly, the mutants lacking all NTRs showed higher photosynthetic efficiency and altered redox states, indicating a functional interaction between chloroplastic and extra-chloroplastic NTRs in photosynthesis regulation. Overall, the NTR system plays a previously unknown role in regulating sink leaf metabolism and plant acclimation to high CO2.