Regulation of cyclic electron flow by chloroplast NADPH-dependent thioredoxin system.

Lauri Nikkanen,Mikko Tikkanen,Eevi Rintamäki,Manuel Guinea Diaz,Andrea Trotta,Eva‐Mari Aro,Jouni Toivola

doi:10.1002/pld3.93

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.

Highlights

In their natural habitats, plants face constant fluctuation of light intensity, including both seasonal changes in photoperiod and daily fluctuations according to environmental conditions
These results are in agreement with the hypothesis that NADPH-thioredoxin reductase (NTRC) acts as a thiol regulator of photosynthesis and chloroplast metabolism in darkness and low light conditions (Nikkanen et al, 2016; Carrillo et al, 2016; Thormählen et al, 2017)
We have shown that the chloroplast NADPH-dependent thioredoxin system (NTRC) stimulates cyclic electron flow around PSI by activating the thylakoid NADH-dehydrogenase-like complex (NDH) complex

Summary

Introduction

Plants face constant fluctuation of light intensity, including both seasonal changes in photoperiod and daily fluctuations according to environmental conditions. Light drives the electron flow from water through PSII, plastoquinone (PQ), cytochrome b6f, plastocyanin (PC) and PSI to ferredoxin and to NADP+, producing NADPH. These photosynthetic electron transfer reactions are coupled to ATP synthesis via translocation of protons to the thylakoid lumen, generating a proton gradient over the thylakoid membrane (ΔpH), which together with membrane potential (ΔΨ) constitutes the proton motive force (pmf) (Hangarter and Good, 1982; Armbruster et al, 2017). Other regulatory mechanisms include the reversible rearrangements of light harvesting complexes to balance the excitation of PSII and PSI known as state transitions (Tikkanen et al, 2006; Ruban and Johnson, 2009; Rochaix, 2011) as well as cyclic electron flow around PSI (CEF), a process where electrons are transferred from ferredoxin back to the PQ pool. CEF has been shown to be important for controlling the magnitude of the pmf (Wang et al, 2015; Shikanai and Yamamoto, 2017), and during induction of photosynthesis (Joliot and Joliot, 2002; Fan et al, 2007). Fan et al (2007) calculated that CEF contributes a maximum of 68% of total electron flux after 30 s illumination of spinach leaves with red and far red light

Results

Discussion

Conclusion