Plant thioredoxins (TRXs) are involved in numerous metabolic and signalling pathways, such as light‐dependent regulation of photosynthesis. The atypical TRX CDSP32, chloroplastic drought‐induced stress protein of 32 kDa, includes two TRX‐fold domains and participates in responses to oxidative stress as an electron donor to other thiol reductases. Here, we further characterised potato lines modified for CDSP32 expression to clarify the physiological roles of the TRX. Upon high salt treatments, modified lines displayed changes in the abundance and redox status of CDSP32 antioxidant partners, and exhibited sensitivity to combined saline‐alkaline stress. In non‐stressed plants overexpressing CDSP32, a lower abundance of photosystem II subunits and ATP‐synthase γ subunit was noticed. The CDSP32 co‐suppressed line showed altered chlorophyll a fluorescence induction and impaired regulation of the transthylakoid membrane potential during dark/light and light/dark transitions. These data, in agreement with the previously reported interaction between CDSP32 and ATP‐synthase γ subunit, suggest that CDSP32 affects the redox regulation of ATP‐synthase activity. Consistently, modelling of protein complex 3‐D structure indicates that CDSP32 could constitute a suitable partner of ATP‐synthase γ subunit. We discuss the roles of the TRX in the regulation of both photosynthetic activity and enzymatic antioxidant network in relation with environmental conditions.