PGR5-Dependent Cyclic Electron Flow Protects Photosystem I under Fluctuating Light at Donor and Acceptor Sides

Abstract

In response to a sudden increase in light intensity, plants must cope with absorbed excess photon energy to protect photosystems from photodamage. Under fluctuating light, PSI is severely photodamaged in the Arabidopsis (Arabidopsis thaliana) proton gradient regulation5 (pgr5) mutant defective in the main pathway of PSI cyclic electron transport (CET). Here, we aimed to determine how PSI is protected by two proposed regulatory roles of CET via transthylakoid DpH formation: (1) reservation of electron sink capacity by adjusting the ATP/NADPH production ratio (acceptor-side regulation) and (2) downregulation of the cytochrome b 6 f complex activity called photosynthetic control for slowing down the electron flow toward PSI (donor-side regulation). We artificially enhanced donor-and acceptor-side regulation in the wild-type and pgr5 backgrounds by introducing the pgr1 mutation conferring the hypersensitivity of the cytochrome b 6 f complex to luminal acidification and moss Physcomitrella patens flavodiiron protein genes, respectively. Enhanced photosynthetic control partially alleviated PSI photodamage in the pgr5 mutant background but restricted linear electron transport under constant high light, suggesting that the strength of photosynthetic control should be optimized. Flavodiiron protein-dependent oxygen photoreduction formed a large electron sink and alleviated PSI photoinhibition, accompanied by the induction of photosynthetic control. Thus, donor-side regulation is essential for PSI photoprotection but acceptor-side regulation also is important to rapidly induce donor-side regulation. In angiosperms, PGR5-dependent CET is required for both functions.Light reactions of photosynthesis convert solar energy into chemical energy in the forms of NADPH and ATP, which are required for CO 2 fixation by the Calvin-Benson cycle. Linear electron transport (LET) from water to NADP + generates both NADPH and ATP, whereas cyclic electron transport (CET) around PSI preferentially contributes to ATP synthesis. In LET, electrons derived from water splitting in PSII are transported to PSI via plastoquinone (PQ), the cytochrome b 6 f (Cyt b 6 f) complex, and plastocyanin. PSI reduces ferredoxin (Fd), an iron-sulfur electron carrier protein, which donates electrons to NADP + via Fd: NADP + oxidoreductase. Coupled with the electron transport, protons (H + ) are concentrated in the thylakoid lumen by H + translocation from the stroma to the thylakoid lumen via the quinone (Q) cycle in the Cyt b 6 f complex and by water splitting in PSII, resulting in the generation of the proton motive force (pmf) composed of a transthylakoid proton gradient (DpH) and a membrane potential (DC; Kramer et al.

Photosynthetic Response Mechanism of Soil Salinity-Induced Cross-Tolerance to Subsequent Drought Stress in Tomato Plants

“…The photoprotective role of CEF has been widely reported to participate in coping with high light, heat, and chilling stress [25]. CEF is required for both the donor-side and acceptor-side regulation and contribute to pmf formation, essential for PSI photoprotection [26,27]. Results of the present study clearly indicated that the soil salinity pretreatment is important for maintaining cyclic electron transfer around PSI.…”

Photorespiration Enhances Acidification of the Thylakoid Lumen, Reduces the Plastoquinone Pool, and Contributes to the Oxidation of P700 at a Lower Partial Pressure of CO2 in Wheat Leaves

“…Furthermore, we recently found that the LEF rate and Fd oxidation rate have a similar relationship to that between the LEF rate and Jg [38]. These results show that ferredoxin (Fd)-dependent CEF [40][41][42][43][44][45][46] is negligibly small; that is, photosynthetic LEF is responsible for the majority of ∆pH formation [38]. The induction mechanism of ∆pH formation across the thylakoid membranes is shown in the following manner: ∆pH formation is observed as an ECS signal increase [26,47].…”

Two dominant boreal conifers use contrasting mechanisms to reactivate photosynthesis in the spring

“…The recent finding that FLV functions as electron acceptor and can reduce O 2 and protect PSI from damage in gymnosperms suggests that this may be one of the key mechanisms facilitating the evergreen lifestyle of boreal conifers [32][33][34] . Angiosperms lack FLV 34,35 and heterologous expression of FLVs in angiosperms have demonstrated complementary functions of the different AEF components 18,19 . However, those measurements were performed on material grown under optimal conditions in climate chambers, similar to the summer samples in our experiments (Figs.…”