The NADPH thioredoxin reductase C functions as an electron donor to 2-Cys peroxiredoxin in a thermophilic cyanobacterium Thermosynechococcus elongatus BP-1

Sueoka, Keigo; Yamazaki, Teruaki; Hiyama, Tetsuo; Nakamoto, Hitoshi

doi:10.1016/j.bbrc.2009.01.091

Cited by 10 publications

(9 citation statements)

References 23 publications

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“…1B, lanes 1 and 2), implying that these proteins can receive reducing power directly from the NTR domain without passing through the Trx domain. In fact, a previous study reported that the Trx domain active site is dispensable for NTRC-dependent 2-Cys Prx reduction in a thermophilic cyanobacterium (28). We validated this possibility using a series of NTRC variant proteins, in which redox-active Cys pairs conserved in the NTR domain and/or Trx domain were substituted with Ser (NTRC C217S/C220S , NTRC C454S/C457S , and NTRC C217S/C220S/C454S/ C457S ).…”

Section: Ntr and Trx Domains Are Both Necessary For Ntrc-dependent Redoxmentioning

confidence: 86%

Two distinct redox cascades cooperatively regulate chloroplast functions and sustain plant viability

Yoshida

Hisabori

2016

Proc. Natl. Acad. Sci. U.S.A.

123

182

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The thiol-based redox regulation system is believed to adjust chloroplast functions in response to changes in light environments. A redox cascade via the ferredoxin-thioredoxin reductase (FTR)/thioredoxin (Trx) pathway has been traditionally considered to serve as a transmitter of light signals to target enzymes. However, emerging data indicate that chloroplasts have a complex redox network composed of diverse redox-mediator proteins and target enzymes. Despite extensive research addressing this system, two fundamental questions are still unresolved: How are redox pathways orchestrated within chloroplasts, and why are chloroplasts endowed with a complicated redox network? In this report, we show that NADPH-Trx reductase C (NTRC) is a key redox-mediator protein responsible for regulatory functions distinct from those of the classically known FTR/Trx system. Target screening and subsequent biochemical assays indicated that NTRC and the Trx family differentially recognize their target proteins. In addition, we found that NTRC is an electron donor to Trx-z, which is a key regulator of gene expression in chloroplasts. We further demonstrate that cooperative control of chloroplast functions via the FTR/Trx and NTRC pathways is essential for plant viability. Arabidopsis double mutants impaired in FTR and NTRC expression displayed lethal phenotypes under autotrophic growth conditions. This severe growth phenotype was related to a drastic loss of photosynthetic performance. These combined results provide an expanded map of the chloroplast redox network and its biological functions.T o preserve the integrity and efficiency of photosynthesis and other metabolic reactions, chloroplast enzymes need to be flexibly and appropriately controlled in response to changes in light environments. The photosynthetic electron transport chain in the chloroplast thylakoid membrane converts light energy into chemical energy, which is captured and stored in ATP and NADPH. These molecules are primarily consumed by the Calvin-Benson cycle in the stroma, but part of the reducing power is used for other metabolic reactions in chloroplasts (e.g., nitrogen and sulfur metabolism). One pathway for the reducing power is the redox cascade, mediated by ferredoxin-thioredoxin reductase (FTR) and thioredoxin (Trx). In this system, FTR receives reducing power from the light-driven photosynthetic electron transport chain via ferredoxin and then donates the reducing power to Trx. A reduced form of Trx subsequently transfers reducing power to target proteins through a dithiol-disulfide exchange reaction, allowing the targets to modulate the enzymatic activities. The redox cascade via the FTR/Trx pathway provides the basis for thiol-based redox regulation in chloroplasts and ensures light-responsive control of chloroplast functions (1, 2).The FTR/Trx pathway has been considered the only pathway regulating redox reactions in chloroplasts. Information about its target proteins has also been limited to a specific set of lightactivated enzymes, such as some enzy...

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Section: Ntr and Trx Domains Are Both Necessary For Ntrc-dependent Redoxmentioning

confidence: 86%

Two distinct redox cascades cooperatively regulate chloroplast functions and sustain plant viability

Yoshida

Hisabori

2016

Proc. Natl. Acad. Sci. U.S.A.

123

182

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“…4), thus showing the same behavior as the plant enzyme. Moreover, whereas the T. elongatus NTRC was reported to oxidize NADH (Sueoka et al, 2009), the Anabaena NTRC shared with the plant enzyme its specificity for NADPH as a source of reducing power (Fig. 4), once again emphasizing its close relationship with the plant enzyme.…”

Section: Discussionmentioning

confidence: 99%

“…To our knowledge, the only NTRC so far described from cyanobacteria is the Thermosynechococcus elongatus enzyme (Sueoka et al, 2009). In this thermophilic cyanobacterium, NTRC was identified as a component of an NAD(P)H oxidase complex induced by oxidative stress, which also contained 2-Cys Prx.…”

Section: Discussionmentioning

confidence: 99%

“…This result indicates that the cyanobacterial enzyme might act as a reductant of 2-Cys Prx and, thus, may function as an antioxidant system, as initially proposed for the enzyme in plant chloroplasts. However, the NTRC from T. elongatus seems to have a reaction mechanism different from that of the plant enzyme, as suggested by the fact that a mutant variant at the active site of the Trx domain of this enzyme was active (Sueoka et al, 2009). In contrast with this result, the analysis of mutant variants at the active site of either the NTR or Trx domain of the Anabaena enzyme completely lost activity (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, in the cyanobacterium Thermosynechococcus elongatus, NTRC was identified as a component of a protein complex showing NAD(P)H oxidase activity. The other component of this complex, which is induced by oxidative stress, was identified as the 2-Cys Prx (Sueoka et al, 2009). The tight association of NTRC with 2-Cys Prx in this cyanobacterium suggests that, as occurs in plant chloroplasts, NTRC acts as an efficient reductant of 2-Cys Prxs, thus serving as an antioxidant system.…”

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confidence: 99%

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A Comparative Analysis of the NADPH Thioredoxin Reductase C-2-Cys Peroxiredoxin System from Plants and Cyanobacteria

et al. 2011

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Redox regulation based on disulfide-dithiol conversion catalyzed by thioredoxins is an important component of chloroplast function. The reducing power is provided by ferredoxin reduced by the photosynthetic electron transport chain. In addition, chloroplasts are equipped with a peculiar NADPH-dependent thioredoxin reductase, termed NTRC, with a joint thioredoxin domain at the carboxyl terminus. Because NADPH can be produced by the oxidative pentose phosphate pathway during the night, NTRC is important to maintain the chloroplast redox homeostasis under light limitation. NTRC is exclusive for photosynthetic organisms such as plants, algae, and some, but not all, cyanobacteria. Phylogenetic analysis suggests that chloroplast NTRC originated from an ancestral cyanobacterial enzyme. While the biochemical properties of plant NTRC are well documented, little is known about the cyanobacterial enzyme. With the aim of comparing cyanobacterial and plant NTRCs, we have expressed the full-length enzyme from the cyanobacterium Anabaena species PCC 7120 as well as site-directed mutant variants and truncated polypeptides containing the NTR or the thioredoxin domains of the protein. Immunological and kinetic analysis showed a high similarity between NTRCs from plants and cyanobacteria. Both enzymes efficiently reduced 2-Cys peroxiredoxins from plants and from Anabaena but not from the cyanobacterium Synechocystis. Arabidopsis (Arabidopsis thaliana) NTRC knockout plants were transformed with the Anabaena NTRC gene. Despite a lower content of NTRC than in wildtype plants, the transgenic plants showed significant recovery of growth and pigmentation. Therefore, the Anabaena enzyme fulfills functions of the plant enzyme in vivo, further emphasizing the similarity between cyanobacterial and plant NTRCs.

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Thiol-based Redox Regulation in Plant Chloroplasts

Yoshida

Hisabori

2019

Signaling and Communication in Plants

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The NADPH thioredoxin reductase C functions as an electron donor to 2-Cys peroxiredoxin in a thermophilic cyanobacterium Thermosynechococcus elongatus BP-1

Cited by 10 publications

References 23 publications

Two distinct redox cascades cooperatively regulate chloroplast functions and sustain plant viability

Two distinct redox cascades cooperatively regulate chloroplast functions and sustain plant viability

A Comparative Analysis of the NADPH Thioredoxin Reductase C-2-Cys Peroxiredoxin System from Plants and Cyanobacteria

Thiol-based Redox Regulation in Plant Chloroplasts

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