NTRC-dependent redox balance of 2-Cys peroxiredoxins is needed for optimal function of the photosynthetic apparatus

Pérez-Ruiz, Juan Manuel; Naranjo, Belén; Ojeda, Valle; Guinea, Manuel; Cejudo, Francisco Javier

doi:10.1073/pnas.1706003114

Cited by 122 publications

(198 citation statements)

References 39 publications

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“…Our results support the model proposed by P erez-Ruiz et al [12], and expanded the view on the regulatory action of the NTRC-2CP system to the stability and function of TBS enzymes. According to this model, oxidized 2CPs, which accumulate in plants devoid of NTRC, act as a relevant sink for electrons from TRXs.…”

Section: Discussionsupporting

confidence: 92%

Redox‐control of chlorophyll biosynthesis mainly depends on thioredoxins

et al. 2018

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In order to maintain enzyme stability and activity, chloroplasts use two systems of thiol-disulfide reductases for the control of redox-dependent properties of proteins. Previous studies have revealed that plastid-localized thioredoxins (TRX) and the NADPH-dependent thioredoxin reductase C (NTRC) are important for the reduction of cysteine residues of enzymes involved in chlorophyll synthesis. Very recently, it was shown that the pale green phenotype of the ntrc mutant is suppressed when the contents of 2-cysteine peroxiredoxins (2CP) A and B are decreased. Here, we show that suppression of the ntrc phenotype results from a recovery of wild-type-like redox control of chlorophyll biosynthesis enzymes in ntrc/2cp mutants. The presented results support the conclusion that TRXs rather than NTRC are the predominant reductases mediating the redox-regulation of these enzymes.

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Section: Discussionsupporting

confidence: 92%

Redox‐control of chlorophyll biosynthesis mainly depends on thioredoxins

et al. 2018

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“…A full list of identified peptides is provided in Supporting Information , while Supporting Information lists 100 chloroplast proteins in order of their abundance in WT and OE‐NTRC eluates but missing in ntrc eluates. Among these proteins were several TRX interactors identified in previous studies (Balmer et al., ; Marchand et al., ; Hall et al., ), as well as established NTRC target proteins such as 2‐cysteine peroxiredoxins (Pérez‐Ruiz et al., ) and enzymes involved in chlorophyll biosynthesis (Richter et al., ). Relevantly in the current context, several proteins involved in CEF around PSI were identified by the Co‐IP/MS screening (Table ).…”

Section: Resultsmentioning

confidence: 99%

“…In a short photoperiod, the ntrc plants have a highly pleiotropic phenotype (Supporting Information ) (Kirchsteiger et al., ; Naranjo et al., ; Nikkanen et al., ; Pérez‐Ruiz et al., Pulido et al., ; Thormählen et al., ) that complicates the interpretation of results from the ntrc line. The high, slow‐rising PIFR and increased dark‐reduction of PQ in short‐day grown ntrc (Figures a and g) were likely caused by a high NPQ (Supporting Information ) and its relaxation in darkness, lowered PSI content (Figure ) (Thormählen et al., ), and impaired stromal redox metabolism (Nikkanen et al., ; Pérez‐Ruiz et al., ). Furthermore, we observed increased accumulation of reduced Fd, the substrate of the NDH complex, in ntrc (Figure d), which may be due to lower activity of CBC enzymes and consequent lower consumption of NADPH in carbon fixation (Nikkanen et al., ).…”

Section: Discussionmentioning

confidence: 99%

“…NTRC has a less negative midpoint redox potential than FTR (Hirasawa et al., ; Yoshida & Hisabori, ) and plays an important regulatory role under low irradiance, while the FTR‐dependent system probably requires more extensive illumination to be fully activated (Geigenberger, Thormählen, Daloso, & Fernie, ; Nikkanen et al., ; Thormählen et al., ). Recent studies have revealed a significant functional overlap and crosstalk between the two chloroplast TRX systems, and indicated that they cooperatively regulate ATP synthesis, the CBC, starch synthesis, and scavenging of reactive oxygen species (ROS) (Geigenberger et al., ; Nikkanen et al., ; Pérez‐Ruiz, Naranjo, Ojeda, Guinea, & Cejudo, ; Thormählen et al., ).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2018

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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.

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“…NTRC has been demonstrated to be a crucial regulator of photosynthesis, chloroplast metabolism and reactive oxygen species (ROS) detoxification (Pérez‐Ruiz et al , Michalska et al , Richter et al , Carrillo et al , Naranjo et al , Nikkanen et al ). Crosstalk and partial redundancy between the two TRX systems exist in the control of photosynthesis and ROS metabolism (Toivola et al , Thormählen et al , Nikkanen et al , Pérez‐Ruiz et al ), but both systems are essential for normal growth and development of plants (Serrato et al , Wang et al ).…”

Section: Introductionmentioning

confidence: 99%

Multilevel regulation of non‐photochemical quenching and state transitions by chloroplast NADPH‐dependent thioredoxin reductase

Nikkanen

Díaz

Toivola

et al. 2019

Physiologia Plantarum

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In natural growth habitats, plants face constant, unpredictable changes in light conditions. To avoid damage to the photosynthetic apparatus on thylakoid membranes in chloroplasts, and to avoid wasteful reactions, it is crucial to maintain a redox balance both within the components of photosynthetic electron transfer chain and between the light reactions and stromal carbon metabolism under fluctuating light conditions. This requires coordinated function of the photoprotective and regulatory mechanisms, such as non‐photochemical quenching (NPQ) and reversible redistribution of excitation energy between photosystem II (PSII) and photosystem I (PSI). In this paper, we show that the NADPH‐dependent chloroplast thioredoxin system (NTRC) is involved in the control of the activation of these mechanisms. In plants with altered NTRC content, the strict correlation between lumenal pH and NPQ is partially lost. We propose that NTRC contributes to downregulation of a slow‐relaxing constituent of NPQ, whose induction is independent of lumenal acidification. Additionally, overexpression of NTRC enhances the ability to adjust the excitation balance between PSII and PSI, and improves the ability to oxidize the electron transfer chain during changes in light conditions. Thiol regulation allows coupling of the electron transfer chain to the stromal redox state during these changes.

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NTRC-dependent redox balance of 2-Cys peroxiredoxins is needed for optimal function of the photosynthetic apparatus

Cited by 122 publications

References 39 publications

Redox‐control of chlorophyll biosynthesis mainly depends on thioredoxins

Redox‐control of chlorophyll biosynthesis mainly depends on thioredoxins

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

Multilevel regulation of non‐photochemical quenching and state transitions by chloroplast NADPH‐dependent thioredoxin reductase

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