Flavodiiron Protein Substitutes for Cyclic Electron Flow without Competing CO<sub>2</sub> Assimilation in Rice

Wada, Shin‐Ichiro; Yamamoto, Hiroshi; Suzuki, Yoshiichi; Yamori, Wataru; Shikanai, Toshiharu; Makino, Amane

doi:10.1104/pp.17.01335

Cited by 93 publications

(74 citation statements)

References 46 publications

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“…DpH formed by CET contributes to additional ATP production to satisfy the ATP/ NADPH production ratio for CO 2 fixation. Consistent with this idea, CO 2 assimilation in rice (Oryza sativa) mutants defective in the PGR5/PGRL1-dependent CET or both CET pathways is disturbed significantly (Nishikawa et al, 2012;Wada et al, 2018).…”

mentioning

confidence: 68%

“…Flv significantly contributes to photoprotection as an electron sink in cyanobacteria, green algae, liverworts, and mosses (Allahverdiyeva et al, 2013;Gerotto et al, 2016;Chaux et al, 2017;Shimakawa et al, 2017). We previously showed that the introduction of P. patens FlvA and FlvB genes significantly alleviates PSI photodamage in fluctuating light in Arabidopsis (Yamamoto et al, 2016) and rice (Wada et al, 2018).…”

Section: Artificial Enhancement Of Electron Sink Capacity By Flv Suppmentioning

confidence: 99%

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

2018

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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.

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confidence: 68%

Section: Artificial Enhancement Of Electron Sink Capacity By Flv Suppmentioning

confidence: 99%

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

2018

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“…Interestingly, Yamamoto et al () reported that the overexpression of flavodiiron protein (Flv) in pgr5 in Arabidopsis recovers ΔY(I). Wada et al () also reported that ΔY(I) is recovered in pgr5 and crr6 double mutant owing to the overexpression of Flv in rice. Flv contributes to oxidize PSI by passing electrons from PSI to O 2 (Helman et al , Shimakawa et al , , Takagi et al ).…”

Section: Discussionmentioning

confidence: 92%

“…Furthermore, ΔY(I) would be independent of CEF‐PSI because Flv stimulates LEF. Importantly, the overexpression of Flv recovers Y(ND) in pgr5 mutant of Arabidopsis, and in pgr5 and crr6 double mutant of rice (Yamamoto et al , Wada et al ). These results strongly support our hypothesis that ΔY(I) strongly relates to Y(ND).…”

Section: Discussionmentioning

confidence: 99%

PROTON GRADIENT REGULATION 5 supports linear electron flow to oxidize photosystem I

Takagi

Miyake

2018

Physiologia Plantarum

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In higher plants, light drives the linear photosynthetic electron transport reaction from H O to electron sinks, which is called the linear electron flow (LEF). LEF activity should be regulated depending on electron sinks; otherwise excess electrons accumulate in the thylakoid membranes and stimulate reactive oxygen species (ROS) production in photosystem I (PSI), which causes oxidative damage to PSI. To prevent ROS production in PSI, PSI should be oxidized during photosynthesis, and PROTON GRADIENT REGULATION 5 (PGR5) and PGR like 1 (PGRL1) are important for this oxidation. PGR5 and PGRL1 are recognized as a component of ferredoxin-dependent cyclic electron flow around PSI (Fd-CEF-PSI), however there is no direct evidence for the significant operation of Fd-CEF-PSI during photosynthesis in wild-type (WT) plants. Thus, electron distribution by PGR5 and PGRL1 between Fd-CEF-PSI and LEF is still elusive. Here, we show direct evidence that Fd-CEF-PSI activity is minor during steady-state photosynthesis by measuring the Fd redox state in vivo in Arabidopsis thaliana. We found that Fd oxidation rate is determined by LEF activity during steady-state photosynthesis in WT. On the other hand, pgr5 and pgrl1 showed lower electron transport efficiency from PSI to electron sinks through Fd during steady-state photosynthesis. These results demonstrate that electrons are exclusively consumed in electron sinks through Fd, and the phenotypes of pgr5 and pgrl1 are likely caused by the disturbance of the LEF between PSI and electron sinks. We suggest that PGR5 and PGRL1 modulate the LEF according to electron sink activities around PSI.

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“…() confirmed this important function of FDPs also in C. reinhardtii . Additionally, it has been shown that P. patens FDPs are able to function also in A. thaliana and rice, and that they can partially compensate for the loss of PGR5 (Yamamoto et al ., ; Wada et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Hunting the main player enabling Chlamydomonas reinhardtii growth under fluctuating light

et al. 2018

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SUMMARYPhotosynthetic organisms have evolved numerous photoprotective mechanisms and alternative electron sinks/pathways to fine-tune the photosynthetic apparatus under dynamic environmental conditions, such as varying carbon supply or fluctuations in light intensity. In cyanobacteria flavodiiron proteins (FDPs) protect the photosynthetic apparatus from photodamage under fluctuating light (FL). In Arabidopsis thaliana, which does not possess FDPs, the PGR5-related pathway enables FL photoprotection. The direct comparison of the pgr5, pgrl1 and flv knockout mutants of Chlamydomonas reinhardtii grown under ambient air demonstrates that all three proteins contribute to the survival of cells under FL, but to varying extents. The FDPs are crucial in providing a rapid electron sink, with flv mutant lines unable to survive even mild FL conditions. In contrast, the PGRL1 and PGR5-related pathways operate over relatively slower and longer timescales. Whilst deletion of PGR5 inhibits growth under mild FL, the pgrl1 mutant line is only impacted under severe FL conditions. This suggests distinct roles, yet a close relationship, between the function of PGR5, PGRL1 and FDP proteins in photoprotection.

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Flavodiiron Protein Substitutes for Cyclic Electron Flow without Competing CO₂ Assimilation in Rice

Cited by 93 publications

References 46 publications

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

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

PROTON GRADIENT REGULATION 5 supports linear electron flow to oxidize photosystem I

Hunting the main player enabling Chlamydomonas reinhardtii growth under fluctuating light

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Flavodiiron Protein Substitutes for Cyclic Electron Flow without Competing CO2 Assimilation in Rice

Cited by 93 publications

References 46 publications

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

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

PROTON GRADIENT REGULATION 5 supports linear electron flow to oxidize photosystem I

Hunting the main player enabling Chlamydomonas reinhardtii growth under fluctuating light

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Flavodiiron Protein Substitutes for Cyclic Electron Flow without Competing CO₂ Assimilation in Rice