Chloroplastic thioredoxin <i>m</i> functions as a major regulator of Calvin cycle enzymes during photosynthesis <i>in vivo</i>

Okegawa, Yuki; Motohashi, Ken

doi:10.1111/tpj.13049

Cited by 96 publications

(94 citation statements)

References 71 publications

(120 reference statements)

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“…7 and Fig. S8D), the Trx-z redox state in vivo could not be determined in this study, at least partly due to the low expression level in mature leaves (40,52,56) and the smeared nature of the protein band in the immunoblotting analysis (Figs. S8B and S9C).…”

Section: Cooperative Redox Regulation By the Ftr/trx And Ntrc Pathwaymentioning

confidence: 85%

“…What is the significance of chloroplast redox regulation in vivo? To address this question, a number of studies using FTR (48,49), Trx (24,35,(50)(51)(52)(53), or NTRC (15,16,27,54) mutant plants have been reported even during the last few years. Most of these studies focused on the in vivo function of individual redox-mediator proteins.…”

Section: Cooperative Redox Regulation By the Ftr/trx And Ntrc Pathwaymentioning

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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Section: Cooperative Redox Regulation By the Ftr/trx And Ntrc Pathwaymentioning

confidence: 85%

Section: Cooperative Redox Regulation By the Ftr/trx And Ntrc Pathwaymentioning

confidence: 99%

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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“…S7). The severe growth phenotype also can likely be explained by the defect in plastid redox status, which also controls photosynthetic electron transport, biogenesis of PSII, activation of Calvin cycle enzymes, and starch synthesis in quadruple silencing plants (Michalska et al, 2009;Lepistö et al, 2013;Wang et al, 2013;Okegawa and Motohashi, 2015;Thormählen et al, 2015). Moreover, a double mutant lacking FTRb and NTRC shows a lethal phenotype on soil and is only viable on Murashige and Skoog medium supplemented with Suc.…”

Section: Impact Of Insufficient Content Of Trx Isoforms and Ntrc On Omentioning

confidence: 99%

“…Numerous in vitro and in vivo studies have shown that TRX f and TRX m are required for multiple metabolic processes in chloroplasts, including the Calvin-Benson cycle (Collin et al, 2003;Michelet et al, 2013;Okegawa and Motohashi, 2015;Yoshida et al, 2015), ATP synthesis (Schwarz et al, 1997) and NADPH export (Wolosiuk et al, 1979;Lara et al, 1980), starch metabolism (Fu et al, 1998;Mikkelsen et al, 2005;Seung et al, 2013;Thormählen et al, 2013), fatty acid synthesis (Sasaki et al, 1997), amino acid synthesis (Balmer et al, 2003), and chlorophyll (Chl) synthesis (Ikegami et al, 2007;Luo et al, 2012). Functional genetic analyses have shown that TRX m4 knockout mutants were affected in cyclic electron flow around PSI (Courteille et al, 2013), while a TRX m3 knockout mutant was affected in meristem development (BenitezAlfonso et al, 2009).…”

mentioning

confidence: 99%

“…Arabidopsis (Arabidopsis thaliana) lines with combined silencing of TRX m1, m2, and m4 were defective in the biogenesis of PSII (Wang et al, 2013). A recent study suggested that TRX m plays a more important role than TRX f in the activation of Fru-1,6-bisphosphatase (FBPase) and sedoheptulose-1,7-bisphosphatase during carbon assimilation (Okegawa and Motohashi, 2015). TRXs also function in the dynamic acclimation of photosynthesis in fluctuating light (Thormahlen et al, 2017).…”

mentioning

confidence: 99%

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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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Comparative analysis of sipeimine content, metabolome and chloroplast genome in cultivated and wild varieties of Fritillaria taipaiensis

Xu,

Chen,

Cai

et al. 2024

J Sci Food Agric

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BACKGROUNDThe wild variety Fritillaria taipaiensis E. B (EB) is known for its superior therapeutic effects, but its limited production cannot meet the demands. As a result, the cultivated variety F. taipaiensis P. Y. Li (PY) has been widely grown. In this study, we conducted a comprehensive analysis comparing EB and PY in terms of external features, Sipeimine content, metabolome, and chloroplast genome to differentiate these two varieties.RESULTSOur research revealed that the petals and pods of EB are green, while those of PY have purple markings. The bulbs of EB contain significantly higher levels of Sipeimine compared to PY. Metabolomic analysis identified 56 differentially expressed metabolites (DMs), with 23 upregulated and 33 downregulated in EB bulbs. Particularly, 3‐Hydroxycinnamic acid and Secoxyloganin may serve as distinctive differential metabolites. These DMs were associated with 17 KEGG pathways, including Pyrimidine metabolism, Alanine, Aspartate and Glutamate, and Galactose metabolism. Differences in the length of the chloroplast genome were primarily observed in the LSC region, with the largest variation in the trnH‐GUC~psbA region. The placement of the trnH gene and the rps gene in proximity to the LSC/IRb boundary differs between EB and PY.CONCLUSIONThe results of this study provide valuable insights for the introduction and comprehensive development of wild F. taipaiensis from a scientific perspective.This article is protected by copyright. All rights reserved.

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Chloroplastic thioredoxin m functions as a major regulator of Calvin cycle enzymes during photosynthesis in vivo

Cited by 96 publications

References 71 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

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

Comparative analysis of sipeimine content, metabolome and chloroplast genome in cultivated and wild varieties of Fritillaria taipaiensis

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