Multi‐level regulation of the chloroplast ATP synthase: the chloroplast NADPH thioredoxin reductase C (NTRC) is required for redox modulation specifically under low irradiance

Abstract

SUMMARYThe chloroplast ATP synthase is known to be regulated by redox modulation of a disulfide bridge on the c-subunit through the ferredoxin-thioredoxin regulatory system. We show that a second enzyme, the recently identified chloroplast NADPH thioredoxin reductase C (NTRC), plays a role specifically at low irradiance. Arabidopsis mutants lacking NTRC (ntrc) displayed a striking photosynthetic phenotype in which feedback regulation of the light reactions was strongly activated at low light, but returned to wild-type levels as irradiance was increased. This effect was caused by an altered redox state of the c-subunit under low, but not high, light. The low light-specific decrease in ATP synthase activity in ntrc resulted in a buildup of the thylakoid proton motive force with subsequent activation of non-photochemical quenching and downregulation of linear electron flow. We conclude that NTRC provides redox modulation at low light using the relatively oxidizing substrate NADPH, whereas the canonical ferredoxin-thioredoxin system can take over at higher light, when reduced ferredoxin can accumulate. Based on these results, we reassess previous models for ATP synthase regulation and propose that NTRC is most likely regulated by light. We also find that ntrc is highly sensitive to rapidly changing light intensities that probably do not involve the chloroplast ATP synthase, implicating this system in multiple photosynthetic processes, particularly under fluctuating environmental conditions.

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

“…In ntrc , high steady‐state pmf under low light intensity (Figures e, and a) was likely caused by impaired activation of the chloroplast ATP synthase and the Calvin–Benson cycle as previously reported (Carrillo et al., ; Nikkanen et al., ). Furthermore, exceptionally high NPQ was recorded in the ntrc line, especially at low light (Supporting Information ).…”

“…The ntrc knockout has a stunted and low chlorophyll phenotype, which is particularly severe in plants grown under short photoperiods (Lepistö et al., , ; Pérez‐Ruiz et al., ). The mutant suffers from an impaired ability to activate the ATP synthase and CBC enzymes as well as elevated nonphotochemical quenching (NPQ) (Carrillo, Froehlich, Cruz, Savage, & Kramer, ; Naranjo et al., ; Nikkanen, Toivola, & Rintamäki, ; Thormählen et al., ). In contrast, NTRC overexpression lines (OE‐NTRC), with 15–20 times higher NTRC content compared to WT, show wild‐type–like visible phenotype, enhanced vegetative growth, and increased activation of the ATP synthase and CBC enzymes, particularly in darkness and low light (Nikkanen et al., ; Toivola et al., ).…”

NADPH Thioredoxin Reductase C and Thioredoxins Act Concertedly in Seedling Development

“…4C). Previous reports have shown that the deficiency of NTRC causes the impairment of light utilization and slightly affects the redox state of the g-subunit of ATPase, hence affecting the qE component of NPQ (Carrillo et al, 2016;Naranjo et al, 2016b). Therefore, the combined deficiency of NTRC and f-or x-type Trxs affects the redox regulation of chloroplast metabolic pathways such as the CalvinBenson cycle but also the efficiency of light utilization, which ultimately might be the reason for the severe growth-retarded phenotype shown by the ntrc-trxx and ntrc-trxf1f2 mutants.…”

Chloroplast ATP Synthase Modulation of the Thylakoid Proton Motive Force: Implications for Photosystem I and Photosystem II Photoprotection

“…It has long been known that the chloroplast ATP synthase is regulated by modulation of a cysteine pair located in a regulatory loop in γ-subunit (Ort and Oxborough, 1992), which is modulated by light-induced electron flow from PSI through thioredoxin at high light and the chloroplast NAD(P)H: thioredoxin reductase C (NTRC) at low light (Carrillo et al, 2016). This regulatory mode is proposed to prevent wasteful ATP hydrolysis in the dark (Wu et al, 2007).…”