Regulation of cyclic electron flow by chloroplast NADPH‐dependent thioredoxin system

Abstract

Linear electron transport in the thylakoid membrane drives photosynthetic NADPH and ATP production, while cyclic electron flow ( CEF ) around photosystem I only promotes the translocation of protons from stroma to thylakoid lumen. The chloroplast NADH dehydrogenase‐like complex ( NDH ) participates in one CEF route transferring electrons from ferredoxin back to the plastoquinone pool with concomitant proton pumping to the lumen. CEF has been proposed to balance the ratio of ATP / NADPH production and to control the redox poise particularly in fluctuating light conditions, but the mechanisms regulating the NDH complex remain unknown. We have investigated potential regulation of the CEF pathways by the chloroplast NADPH ‐thioredoxin reductase ( NTRC ) in vivo by using an Arabidopsis knockout line of NTRC as well as lines overexpressing NTRC . Here, we present biochemical and biophysical evidence showing that NTRC stimulates the activity of NDH ‐dependent CEF and is involved in the regulation of generation of proton motive force, thylakoid conductivity to protons, and redox balance between the thylakoid electron transfer chain and the stroma during changes in light conditions. Furthermore, protein–protein interaction assays suggest a putative thioredoxin‐target site in close proximity to the ferredoxin‐binding domain of NDH , thus providing a plausible mechanism for redox regulation of the NDH ferredoxin:plastoquinone oxidoreductase activity.

Multilevel regulation of non‐photochemical quenching and state transitions by chloroplast NADPH‐dependent thioredoxin reductase

“…Moreover, NTRC overexpression significantly enhances, while NTRC knockout impairs, the plant's ability to redistribute excitation energy between PSII and PSI. In conjunction with other recent reports (Naranjo et al , Thormählen et al , Nikkanen et al ), our findings support the hypothesis that NTRC has an important function in adjusting photosynthetic redox poise through either direct or indirect regulation of photoprotective and regulatory mechanisms during changes in light conditions.…”

“…Recent reports on chloroplast TRX systems have emphasized their crucial role in the regulation of processes that allow plants to cope with changes in light conditions (Carrillo et al , Nikkanen et al , Thormählen et al , Da et al , Nikkanen et al ). These include regulatory and photoprotective processes of photosynthetic electron transfer, ATP synthesis as well as carbon fixation and secondary carbon metabolism (for reviews, see Michelet et al , Nikkanen and Rintamäki , Geigenberger et al ).…”

“…These include regulatory and photoprotective processes of photosynthetic electron transfer, ATP synthesis as well as carbon fixation and secondary carbon metabolism (for reviews, see Michelet et al , Nikkanen and Rintamäki , Geigenberger et al ). Accordingly, modifications of TRX activity alter the redox poise between the photosynthetic electron transfer chain and stromal electron sinks (Rey et al , Thormählen et al , Carrillo et al , Nikkanen et al , Thormählen et al , Nikkanen et al ).…”

“…It has recently been proposed that chloroplast TRXs are also major regulators of photosynthetic redox poise during fluctuations in light intensity (Nikkanen and Rintamäki , Thormählen et al , Nikkanen et al ). TRXs control the redox homeostasis between the photosynthetic electron transfer chain in thylakoid membranes (PETC) and stromal processes by reversibly activating and deactivating regulatory and photoprotective mechanisms that prevent excessive reduction of the PETC and damage to the photosynthetic apparatus (Rintamäki et al , Courteille et al , Strand et al , Da et al ).…”

“…Alteration of stromal thiol redox state has been shown to affect NPQ (Naranjo et al , Da et al ), CEF (Courteille et al , Strand et al , Nikkanen et al ) and reversible phosphorylation of LHCII proteins (Rintamäki et al ). TRXs may affect induction of NPQ via inhibition of VDE by TRX‐mediated reduction of regulatory disulfides (Hall et al ), while thiol regulation of ZE has also recently been demonstrated (Da et al ).…”