NADPH Thioredoxin Reductase C Is Localized in Plastids of Photosynthetic and Nonphotosynthetic Tissues and Is Involved in Lateral Root Formation in <i>Arabidopsis</i>

Kirchsteiger, Kerstin; Ferrández, Julia; Pascual, María Belén; González, Maricruz; Cejudo, Francisco Javier

doi:10.1105/tpc.111.092304

Cited by 80 publications

(78 citation statements)

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“…NTRC is exclusive of organisms that perform oxygenic photosynthesis and shows plastid localization in plants (Kirchsteiger et al, 2012). Moreover, biochemical analyses revealed that NTRC is able to conjugate both NTR and Trx activities to efficiently reduce the hydrogen peroxide-scavenging enzyme 2-Cys peroxiredoxin (Moon et al, 2006;Pérez-Ruiz et al, 2006;Alkhalfioui et al, 2007).…”

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NADPH Thioredoxin Reductase C and Thioredoxins Act Concertedly in Seedling Development

et al. 2017

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ORCID IDs: 0000-0001-8141-9679 (M.G.); 0000-0002-9570-9746 (A.J.S.); 0000-0001-9512-349X (P.G.); 0000-0002-3936-5491 (F.J.C.).Thiol-dependent redox regulation of enzyme activity plays a central role in the rapid acclimation of chloroplast metabolism to ever-fluctuating light availability. This regulatory mechanism relies on ferredoxin reduced by the photosynthetic electron transport chain, which fuels reducing power to thioredoxins (Trxs) via a ferredoxin-dependent Trx reductase. In addition, chloroplasts harbor an NADPH-dependent Trx reductase, which has a joint Trx domain at the carboxyl terminus, termed NTRC. Thus, a relevant issue concerning chloroplast function is to establish the relationship between these two redox systems and its impact on plant development. To address this issue, we generated Arabidopsis (Arabidopsis thaliana) mutants combining the deficiency of NTRC with those of Trxs f, which participate in metabolic redox regulation, and that of Trx x, which has antioxidant function. The ntrc-trxf1f2 and, to a lower extent, ntrc-trxx mutants showed severe growth-retarded phenotypes, decreased photosynthesis performance, and almost abolished light-dependent reduction of fructose-1,6-bisphosphatase. Moreover, the combined deficiency of both redox systems provokes aberrant chloroplast ultrastructure. Remarkably, both the ntrc-trxf1f2 and ntrc-trxx mutants showed high mortality at the seedling stage, which was overcome by the addition of an exogenous carbon source. Based on these results, we propose that NTRC plays a pivotal role in chloroplast redox regulation, being necessary for the activity of diverse Trxs with unrelated functions. The interaction between the two thiol redox systems is indispensable to sustain photosynthesis performed by cotyledons chloroplasts, which is essential for early plant development.

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NADPH Thioredoxin Reductase C and Thioredoxins Act Concertedly in Seedling Development

et al. 2017

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“…Only a few targets were shown to be controlled by NTRC. NTRC functions in the abiotic oxidative stress response (Serrato et al, 2004), starch synthesis (Michalska et al, 2009), Chl synthesis Pérez-Ruiz et al, 2014), the Calvin-Benson cycle (Thormählen et al, 2015), lateral root formation in Arabidopsis (Kirchsteiger et al, 2012), nonphotochemical quenching (Naranjo et al, 2016), as a holdase chaperone function enhancing thermotolerance to Arabidopsis (Chae et al, 2013), and as an electron donor of 2-Cys-peroxiredoxin, thus playing a key role in the detoxification of reactive oxygen species (ROS; Pérez-Ruiz et al, 2006;Spínola et al, 2008;Kirchsteiger et al, 2009). Recent research suggested that cooperative control of chloroplast functions via the ferredoxin-thioredoxin reductase (FTR)/TRX and NTRC pathways is essential for plant viability.…”

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Thioredoxin and NADPH-Dependent Thioredoxin Reductase C Regulation of Tetrapyrrole Biosynthesis

Wang

et al. 2017

Plant Physiol.

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In chloroplasts, thioredoxin (TRX) isoforms and NADPH-dependent thioredoxin reductase C (NTRC) act as redox regulatory factors involved in multiple plastid biogenesis and metabolic processes. To date, less is known about the functional coordination between TRXs and NTRC in chlorophyll biosynthesis. In this study, we aimed to explore the potential functions of TRX m and NTRC in the regulation of the tetrapyrrole biosynthesis (TBS) pathway. Silencing of three genes, TRX m1, TRX m2, and TRX m4 (TRX ms), led to pale-green leaves, a significantly reduced 5-aminolevulinic acid (ALA)-synthesizing capacity, and reduced accumulation of chlorophyll and its metabolic intermediates in Arabidopsis (Arabidopsis thaliana). The contents of ALA dehydratase, protoporphyrinogen IX oxidase, the I subunit of Mg-chelatase, Mg-protoporphyrin IX methyltransferase (CHLM), and NADPH-protochlorophyllide oxidoreductase were decreased in triple TRX m-silenced seedlings compared with the wild type, although the transcript levels of the corresponding genes were not altered significantly. Protein-protein interaction analyses revealed a physical interaction between the TRX m isoforms and CHLM. 4-Acetoamido-4-maleimidylstilbene-2,2-disulfonate labeling showed the regulatory impact of TRX ms on the CHLM redox status. Since CHLM also is regulated by NTRC , we assessed the concurrent functions of TRX m and NTRC in the control of CHLM. Combined deficiencies of three TRX m isoforms and NTRC led to a cumulative decrease in leaf pigmentation, TBS intermediate contents, ALA synthesis rate, and CHLM activity. We discuss the coordinated roles of TRX m and NTRC in the redox control of CHLM stability with its corollary activity in the TBS pathway.

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“…Three isoforms of NTR (NTRA, NTRB, and NTRC) are reported in Arabidopsis (Arabidopsis thaliana) that link TRXs to multiple target proteins of metabolic processes. While NTRA and NTRB are dually targeted to cytosol or mitochondria, NTRC is plastid localized and one of the main redox regulators in photosynthetic and nonphotosynthetic active plastids (Serrato et al, 2004;Pérez-Ruiz et al, 2006;Spínola et al, 2008;Kirchsteiger et al, 2009Kirchsteiger et al, , 2012Lepistö et al, 2009;Pulido et al, 2010). NTRC contains a C-terminal TRX domain and acts as a bifunctional enzyme with NTR/TRX activity for the reduction of specific target proteins (Serrato et al, 2004).…”

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Posttranslational Influence of NADPH-Dependent Thioredoxin Reductase C on Enzymes in Tetrapyrrole Synthesis

Richter

Peter²,

Rothbart³

et al. 2013

Plant Physiology

115

112

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The NADPH-dependent thioredoxin reductase C (NTRC) is involved in redox-related regulatory processes in chloroplasts and nonphotosynthetic active plastids. Together with 2-cysteine peroxiredoxin, it forms a two-component peroxide-detoxifying system that acts as a reductant under stress conditions. NTRC stimulates in vitro activity of magnesium protoporphyrin IX monomethylester (MgPMME) cyclase, most likely by scavenging peroxides. Reexamination of tetrapyrrole intermediate levels of the Arabidopsis (Arabidopsis thaliana) knockout ntrc reveals lower magnesium protoporphyrin IX (MgP) and MgPMME steadystate levels, the substrate and the product of MgP methyltransferase (CHLM) preceding MgPMME cyclase, while MgP strongly accumulates in mutant leaves after 5-aminolevulinic acid feeding. The ntrc mutant has a reduced capacity to synthesize 5-aminolevulinic acid and reduced CHLM activity compared with the wild type. Although transcript levels of genes involved in chlorophyll biosynthesis are not significantly altered in 2-week-old ntrc seedlings, the contents of glutamyl-transfer RNA reductase1 (GluTR1) and CHLM are reduced. Bimolecular fluorescence complementation assay confirms a physical interaction of NTRC with GluTR1 and CHLM. While ntrc contains partly oxidized CHLM, the wild type has only reduced CHLM. As NTRC also stimulates CHLM activity in vitro, it is proposed that NTRC has a regulatory impact on the redox status of conserved cysteine residues of CHLM. It is hypothesized that a deficiency of NTRC leads to a lower capacity to reduce cysteine residues of GluTR1 and CHLM, affecting the stability and, thereby, altering the activity in the entire tetrapyrrole synthesis pathway.During the last decades, almost all enzymes of tetrapyrrole biosynthesis and their complex network of transcriptional regulation have been comprehensively studied (Tanaka et al., 2011). These studies revealed a complex control of the expression of genes encoding enzymes in the light-regulated chlorophyll (Chl)-synthesizing branch of tetrapyrrole metabolism. In brief, 5-aminolevulinic acid (ALA) is synthesized in a transfer RNA (tRNA) GLU -mediated pathway, and eight molecules of ALA are ultimately converted in a series of enzymatic steps to protoporphyrin IX. The polymeric magnesium (Mg) chelatase complex consisting of the three different subunits CHLH, CHLI, and CHLD directs protoporphyrin IX into the Mg branch of tetrapyrrole biosynthesis. Methylation of magnesium protoporphyrin (MgP) by MgP methyltransferase (CHLM) at the C13 of pyrrole ring C initiates the formation of the typical fifth ring. The product of this step, magnesium protoporphyrin monomethylester (MgPMME), is then converted to divinyl protochlorophyllide (PChlide) by an oxidative cyclase complex. NADPH:protochlorophyllide oxidoreductase (POR) synthesizes chlorophyllide (Chlide). PChlide and Chlide are most likely the main substrates of a divinyl reductase that reduces the C7-C8 double bond, forming a monovinyl product. The two final steps of Chl a and b synthesis are likely ...

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NADPH Thioredoxin Reductase C Is Localized in Plastids of Photosynthetic and Nonphotosynthetic Tissues and Is Involved in Lateral Root Formation in Arabidopsis

Cited by 80 publications

References 63 publications

NADPH Thioredoxin Reductase C and Thioredoxins Act Concertedly in Seedling Development

NADPH Thioredoxin Reductase C and Thioredoxins Act Concertedly in Seedling Development

Thioredoxin and NADPH-Dependent Thioredoxin Reductase C Regulation of Tetrapyrrole Biosynthesis

Posttranslational Influence of NADPH-Dependent Thioredoxin Reductase C on Enzymes in Tetrapyrrole Synthesis

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