Cyclic Electron Transport around PSI Contributes to Photosynthetic Induction with Thioredoxin <i>f</i>

Okegawa, Yuki; Basso, Leonardo; Shikanai, Toshiharu; Motohashi, Ken

doi:10.1104/pp.20.00741

Cited by 18 publications

(11 citation statements)

References 52 publications

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“…Knocking out the NDH-like CET pathway in the mutant did not alter NPQ kinetics in the moderate PAR levels applied here. In contrast, knocking out PGR5-PGRL1 in the pgrl1ab mutant led to significantly altered NPQ kinetics compared to WT 45-48 .…”

Section: Resultsmentioning

confidence: 80%

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Plants cope with fluctuating light by frequency-dependent non-photochemical quenching and cyclic electron transport

Niu

Lazár

Holzwarth

et al. 2022

Preprint

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Plants are often exposed in nature to light fluctuations with characteristic periods of several seconds to minutes. Photosynthetically active irradiance fluctuates typically in the range of several hundreds of micromol(photons).m-2.s-1. The photosynthetic regulatory networks that are necessary for minimizing damage by the dynamic load between redox reactions in fluctuating light are poorly understood. Arbitrary light fluctuations can be represented by a sum of harmonic oscillations and, to resolve the elemental components of any complex light patterns, we aimed at characterizing photosynthetic reactions in light that oscillated as an elemental sinus function. Chlorophyll fluorescence yield and optical transmission proxies of P700, plastocyanin, and ferredoxin were measured in Arabidopsis thaliana under oscillating light of various frequencies and amplitudes. The role of non-photochemical quenching (NPQ) and of cyclic electron transport around Photosystem I (CET) was studied by comparing the dynamics in wild-type plants with mutants that were deficient in NPQ (npq1 and npq4) or CET (crr2-2 and pgrl1ab). The study revealed a highly contrasting response in the mutants compared to wild type documenting relevance of non-photochemical quenching and cyclic electron transport for the functioning of plants in a dynamic light environment. The mutants deficient in the non-photochemical quenching constituents exhibited forced oscillations of much higher amplitude than those found in the wild types. The contrast was used to identify the range of frequencies (f < 1/60s) in which the non-photochemical quenching was highly effective. The frequency-domain analysis revealed complex resonance behaviors with the 1/30 s-1 and 1/60 s-1 frequencies that were absent in the npq4 mutant and reduced in the npq1 mutant. This contrast suggests an anomalous dynamic behavior of thylakoid acidification and PsbS-dependent feedback downregulation of Photosystem II light-harvesting at these frequencies. The mutants incapacitated in the cyclic electron transport exhibited a distinct dynamic response. The crr2-2 mutant lacks the activity of photosynthetic NADH dehydrogenase-like complex and typically exhibits wild-type-like induction during a dark-light transition and differs in the light-to-dark relaxation in the time domain. It showed a distinct dynamic signature in oscillating light that involved both rising and declining light phases. The pgrl1ab mutant exhibited a contrasting anomalous response to oscillating light, particularly in the redox reactions involving plastocyanin, P700, and ferredoxin. These findings thus suggest a crucial role of cyclic electron transport in the dynamic properties and regulation of the plants in fluctuating irradiance. The finding of contrasting frequency-dependent modes may explain the existence of multiple, seemingly redundant regulatory mechanisms, each presumably protecting the plant in a different frequency range. The study moreover documented that the harmonically oscillating light can serve, in addition to identifying the photosynthetic dynamics in natural fluctuating light, for revealing unique dynamic features in mutants, and, likely, for sensing plant stress. Furthermore, the sensing by harmonic forcing does not require dark-acclimation and may, thus, conveniently monitor the status of photosynthesis of plants in phenotyping platforms, in greenhouses, and in-field.

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Section: Resultsmentioning

confidence: 80%

“…In contrast, knocking out PGR5-PGRL1 in the pgrl1ab mutant led to significantly altered NPQ kinetics compared to WT [45][46][47][48] .…”

Section: Induction Of Npq By Constant Lightmentioning

confidence: 99%

Plants cope with fluctuating light by frequency-dependent non-photochemical quenching and cyclic electron transport

Niu

Lazár

Holzwarth

et al. 2022

Preprint

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“…Therefore, another possibility It has also been shown that Trx m4 forms a complex with PGRL1 and inactivates it [46]. Indeed, phenotypic effects of trx m4 [46,47], but not of other thioredoxin mutants like trx f1f2 [48], can be suppressed by pgr5. Multiple sources of evidence support the notion that chloroplast Fd-FTR-Trxs and NTRC act in a concerted fashion, with 2-Cys Prxs serving as connecting links between the two redox systems [27].…”

Section: Pgrl1 Dimer Formation and Protein Content In The Absence Of Ntrcmentioning

confidence: 99%

NTRC Effects on Non-Photochemical Quenching Depends on PGR5

et al. 2021

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Non-photochemical quenching (NPQ) protects plants from the detrimental effects of excess light. NPQ is rapidly induced by the trans-thylakoid proton gradient during photosynthesis, which in turn requires PGR5/PGRL1-dependent cyclic electron flow (CEF). Thus, Arabidopsis thaliana plants lacking either protein cannot induce transient NPQ and die under fluctuating light conditions. Conversely, the NADPH-dependent thioredoxin reductase C (NTRC) is required for efficient energy utilization and plant growth, and in its absence, transient and steady-state NPQ is drastically increased. How NTRC influences NPQ and functionally interacts with CEF is unclear. Therefore, we generated the A. thaliana line pgr5 ntrc, and found that the inactivation of PGR5 suppresses the high transient and steady-state NPQ and impaired growth phenotypes observed in the ntrc mutant under short-day conditions. This implies that NTRC negatively influences PGR5 activity and, accordingly, the lack of NTRC is associated with decreased levels of PGR5, possibly pointing to a mechanism to restrict upregulation of PGR5 activity in the absence of NTRC. When exposed to high light intensities, pgr5 ntrc plants display extremely impaired photosynthesis and growth, indicating additive effects of lack of both proteins. Taken together, these findings suggest that the interplay between NTRC and PGR5 is relevant for photoprotection and that NTRC might regulate PGR5 activity.

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“…Given TCR has redox-active cysteine residues (Figures 2D and S2B), oxidation and reduction of the disulfide bond may have a role in the TCR function. Electrons derived from Fd are transferred to the thioredoxin system that affects CBB cycle activation as well as CET (Nikkanen et al, 2018;Okegawa and Motohashi, 2020), suggesting that TCR also functionally interacts with the thioredoxin system, through disulfide-bond exchange, to control electron transfer downstream of PSI. The isolated thylakoid membranes of tcr plants showed a WT-like Fd-dependent fluorescent increment both in the presence and absence of AA (Figure S9), suggesting that TCR is not involved in the Fd-dependent CET.…”

Section: Tcr-dependent Electron Transfer Affects Cet Activitymentioning

confidence: 99%

The evolutionary conserved iron-sulfur protein TCR controls P700 oxidation in photosystem I

et al. 2021

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Summary In natural habitats, plants have developed sophisticated regulatory mechanisms to optimize the photosynthetic electron transfer rate at the maximum efficiency and cope with the changing environments. Maintaining proper P700 oxidation at photosystem I (PSI) is the common denominator for most regulatory processes of photosynthetic electron transfers. However, the molecular complexes and cofactors involved in these processes and their function(s) have not been fully clarified. Here, we identified a redox-active chloroplast protein, the triplet-cysteine repeat protein (TCR). TCR shared similar expression profiles with known photosynthetic regulators and contained two triplet-cysteine motifs (CxxxCxxxC). Biochemical analysis indicated that TCR localizes in chloroplasts and has a [3Fe-4S] cluster. Loss of TCR limited the electron sink downstream of PSI during dark-to-light transition. Arabidopsis pgr5-tcr double mutant reduced growth significantly and showed unusual oxidation and reduction of plastoquinone pool. These results indicated that TCR is involved in electron flow(s) downstream of PSI, contributing to P700 oxidation.

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Cyclic Electron Transport around PSI Contributes to Photosynthetic Induction with Thioredoxin f

Cited by 18 publications

References 52 publications

Plants cope with fluctuating light by frequency-dependent non-photochemical quenching and cyclic electron transport

Plants cope with fluctuating light by frequency-dependent non-photochemical quenching and cyclic electron transport

NTRC Effects on Non-Photochemical Quenching Depends on PGR5

The evolutionary conserved iron-sulfur protein TCR controls P700 oxidation in photosystem I

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