A Novel NADPH Thioredoxin Reductase, Localized in the Chloroplast, Which Deficiency Causes Hypersensitivity to Abiotic Stress in Arabidopsis thaliana

Serrato, Antonio Jesús; Pérez-Ruiz, Juan Manuel; Spínola, Mauro de Mesquita; Cejudo, Francisco Javier

doi:10.1074/jbc.m404696200

Cited by 335 publications

(428 citation statements)

References 33 publications

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“…Several differences between NTRC and ACHT1 suggest different roles for the two proteins. NTRC is a soluble stromal protein (Serrato et al, 2004), whereas ACHT1 is mainly associated with the thylakoids (Dangoor et al, 2009). ACHT1 draws its reducing power from photosynthetic linear electron flow, whereas NTRC depends on NADPH, which is produced also in the dark (Pérez-Ruiz et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

A Chloroplast Light-Regulated Oxidative Sensor for Moderate Light Intensity in Arabidopsis

et al. 2012

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The transition from dark to light involves marked changes in the redox reactions of photosynthetic electron transport and in chloroplast stromal enzyme activity even under mild light and growth conditions. Thus, it is not surprising that redox regulation is used to dynamically adjust and coordinate the stromal and thylakoid compartments. While oxidation of regulatory proteins is necessary for the regulation, the identity and the mechanism of action of the oxidizing pathway are still unresolved. Here, we studied the oxidation of a thylakoid-associated atypical thioredoxin-type protein, ACHT1, in the Arabidopsis thaliana chloroplast. We found that after a brief period of net reduction in plants illuminated with moderate light intensity, a significant oxidation reaction of ACHT1 arises and counterbalances its reduction. Interestingly, ACHT1 oxidation is driven by 2-Cys peroxiredoxin (Prx), which in turn eliminates peroxides. The ACHT1 and 2-Cys Prx reaction characteristics in plants further indicated that ACHT1 oxidation is linked with changes in the photosynthetic production of peroxides. Our findings that plants with altered redox poise of the ACHT1 and 2-Cys Prx pathway show higher nonphotochemical quenching and lower photosynthetic electron transport infer a feedback regulatory role for this pathway.

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Section: Discussionmentioning

confidence: 99%

A Chloroplast Light-Regulated Oxidative Sensor for Moderate Light Intensity in Arabidopsis

et al. 2012

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“…NTRC is one of the key redox-mediator proteins, first reported in 2004 (12). NTRC target proteins include 2-Cys Prx (13), AGPase (14), and Mg-chelatase subunits (and perhaps other proteins involved in tetrapyrrole metabolism) (15,16).…”

Section: Ntrc and Five Trx Subtypes Differentially Recognize Target Pmentioning

confidence: 99%

“…NTRC uses NADPH as a source of reducing power, and is thus able to work in the redox regulation independent of the FTR/Trx pathway. NTRC-deficient plants display obvious phenotypes with palegreen leaves (12,13), indicating that NTRC-dependent redox regulation in chloroplasts has an important role in plants. Although target proteins (13)(14)(15)(16) and catalytic mechanisms (17,18) for NTRC have been partly reported to date, its physiological importance, especially in the context of functional differences from the FTR/Trx system, is largely uncharacterized.…”

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confidence: 99%

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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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“…Reverse genetic studies suggest an antioxidant role for the FTR pathway (Keryer et al, 2004). Recently, an atypical bidomain NTR-TRX-like thioredoxin reductase (NTRC) was proposed to relay the FTR detoxification system during the night (Serrato et al, 2004;Perez-Ruiz et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Inactivation of Thioredoxin Reductases Reveals a Complex Interplay between Thioredoxin and Glutathione Pathways in Arabidopsis Development

et al. 2007

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NADPH-dependent thioredoxin reductases (NTRs) are key regulatory enzymes determining the redox state of the thioredoxin system. The Arabidopsis thaliana genome has two genes coding for NTRs (NTRA and NTRB), both of which encode mitochondrial and cytosolic isoforms. Surprisingly, plants of the ntra ntrb knockout mutant are viable and fertile, although with a wrinkled seed phenotype, slower plant growth, and pollen with reduced fitness. Thus, in contrast with mammals, our data demonstrate that neither cytosolic nor mitochondrial NTRs are essential in plants. Nevertheless, in the double mutant, the cytosolic thioredoxin h3 is only partially oxidized, suggesting an alternative mechanism for thioredoxin reduction. Plant growth in ntra ntrb plants is hypersensitive to buthionine sulfoximine (BSO), a specific inhibitor of glutathione biosynthesis, and thioredoxin h3 is totally oxidized under this treatment. Interestingly, this BSO-mediated growth arrest is fully reversible, suggesting that BSO induces a growth arrest signal but not a toxic accumulation of activated oxygen species. Moreover, crossing ntra ntrb with rootmeristemless1, a mutant blocked in root growth due to strongly reduced glutathione synthesis, led to complete inhibition of both shoot and root growth, indicating that either the NTR or the glutathione pathway is required for postembryonic activity in the apical meristem.

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A Novel NADPH Thioredoxin Reductase, Localized in the Chloroplast, Which Deficiency Causes Hypersensitivity to Abiotic Stress in Arabidopsis thaliana

Cited by 335 publications

References 33 publications

A Chloroplast Light-Regulated Oxidative Sensor for Moderate Light Intensity in Arabidopsis

A Chloroplast Light-Regulated Oxidative Sensor for Moderate Light Intensity in Arabidopsis

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

Inactivation of Thioredoxin Reductases Reveals a Complex Interplay between Thioredoxin and Glutathione Pathways in Arabidopsis Development

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