Publishing type：Research paper (scientific journal)   Publisher：Springer Science and Business Media LLC  

Abstract

Thioredoxin (Trx) is a small redox mediator protein involved in the regulation of various chloroplast functions by modulating the redox state of Trx target proteins in ever-changing light environments. Using reducing equivalents produced by the photosynthetic electron transport chain, Trx reduces the disulfide bonds on target proteins and generally turns on their activities. While the details of the protein-reduction mechanism by Trx have been well investigated, the oxidation mechanism that counteracts it has long been unclear. We have recently demonstrated that Trx-like proteins such as Trx-like2 and atypical Cys His-rich Trx (ACHT) can function as protein oxidation factors in chloroplasts. Our latest study on transgenic Arabidopsis plants indicated that the ACHT isoform ACHT2 is involved in regulating the thermal dissipation of light energy. To understand the role of ACHT2 in vivo, we characterized phenotypic changes specifically caused by ACHT2 overexpression in Arabidopsis. ACHT2-overexpressing plants showed growth defects, especially under high light conditions. This growth phenotype was accompanied with the impaired reductive activation of Calvin–Benson cycle enzymes, enhanced thermal dissipation of light energy, and decreased photosystem II activity. Overall, ACHT2 overexpression promoted protein oxidation that led to the inadequate activation of Calvin–Benson cycle enzymes in light and consequently induced negative feedback control of the photosynthetic electron transport chain. This study highlights the importance of the balance between protein reduction and oxidation in chloroplasts for optimal photosynthetic performance and plant growth.

DOI： 10.1007/s10265-024-01519-2

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Other Link： https://link.springer.com/article/10.1007/s10265-024-01519-2/fulltext.html

Authorship：Lead author,　Corresponding author   Publishing type：Research paper (scientific journal)   Publisher：Oxford University Press (OUP)  

Abstract

Various chloroplast proteins are activated/deactivated during the light/dark cycle via the redox regulation system. Although the photosynthetic electron transport chain provides reducing power to redox-sensitive proteins via the ferredoxin (Fd)/thioredoxin (Trx) pathway for their enzymatic activity control, how the redox states of individual proteins are linked to electron transport efficiency remains uncharacterized. Here we addressed this subject with a focus on the photosynthetic induction phase. We used Arabidopsis plants, in which the amount of Fd–Trx reductase (FTR), a core component in the Fd/Trx pathway, was genetically altered. Several chloroplast proteins showed different redox shift responses toward low- and high-light treatments. The light-dependent reduction of Calvin–Benson cycle enzymes fructose 1,6-bisphosphatase (FBPase) and sedoheptulose 1,7-bisphosphatase (SBPase) was partially impaired in the FTR-knockdown ftrb mutant. Simultaneous analyses of chlorophyll fluorescence and P700 absorbance change indicated that the induction of the electron transport reactions was delayed in the ftrb mutant. FTR overexpression also mildly affected the reduction patterns of FBPase and SBPase under high-light conditions, which were accompanied by the modification of electron transport properties. Accordingly, the redox states of FBPase and SBPase were linearly correlated with electron transport rates. In contrast, ATP synthase was highly reduced even when electron transport reactions were not fully induced. Furthermore, the redox response of proton gradient regulation 5-like photosynthetic phenotype1 (PGRL1; a protein involved in cyclic electron transport) did not correlate with electron transport rates. Our results provide insights into the working dynamics of the redox regulation system and their differential associations with photosynthetic electron transport efficiency.

DOI： 10.1093/pcp/pcae013

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Other Link： https://academic.oup.com/pcp/article-pdf/65/5/737/58008537/pcae013.pdf

Publishing type：Research paper (scientific journal)   Publisher：Springer Science and Business Media LLC  

Abstract

Serine metabolism is involved in various biological processes. Here we investigate primary functions of the phosphorylated pathway of serine biosynthesis in a non-vascular plant Marchantia polymorpha by analyzing knockout mutants of MpPGDH encoding 3-phosphoglycerate dehydrogenase in this pathway. Growth phenotypes indicate that serine from the phosphorylated pathway in the dark is crucial for thallus growth. Sperm development requires serine from the phosphorylated pathway, while egg formation does not. Functional MpPGDH in the maternal genome is necessary for embryo and sporophyte development. Under high CO₂ where the glycolate pathway of serine biosynthesis is inhibited, suppressed thallus growth of the mutants is not fully recovered by exogenously-supplemented serine, suggesting the importance of serine homeostasis involving the phosphorylated and glycolate pathways. Metabolomic phenotypes indicate that the phosphorylated pathway mainly influences the tricarboxylic acid cycle, the amino acid and nucleotide metabolism, and lipid metabolism. These results indicate the importance of the phosphorylated pathway of serine biosynthesis in the dark, in the development of sperm, embryo, and sporophyte, and metabolism in M. polymorpha.

DOI： 10.1038/s42003-023-05746-6

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Other Link： https://www.nature.com/articles/s42003-023-05746-6

Authorship：Lead author,　Corresponding author   Publishing type：Research paper (scientific journal)   Publisher：Oxford University Press (OUP)  

Abstract

Thiol/disulfide-based redox regulation is a ubiquitous post-translational protein modification. In plant chloroplasts, this regulatory mechanism is tightly associated with the light-dependent activation of photosynthetic enzymes (e.g. Calvin–Benson cycle enzymes). A thioredoxin (Trx)-mediated pathway was discovered to transmit light signals as a reducing power about half a century ago; since then, it has been accepted as the basic machinery of chloroplast redox regulation. However, during the past two decades, it has been increasingly apparent that plants have acquired multiple Trx isoforms and Trx-like proteins in chloroplasts. Furthermore, proteomics-based analyses have identified various chloroplast enzymes as potential targets of redox regulation. These facts highlight the necessity to revisit the molecular basis and physiological importance of the redox regulation system in chloroplasts. Recent studies have revealed novel aspects of this system, including unprecedented redox-regulated processes in chloroplasts and the functional diversity of Trx family proteins. Of particular significance is the identification of protein-oxidizing pathways that turn off photosynthetic metabolism during light-to-dark transitions. In this review, we summarize current insights into the redox regulation network in chloroplasts.

DOI： 10.1093/pcp/pcad049

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Other Link： https://academic.oup.com/pcp/article-pdf/64/7/704/50898818/pcad049.pdf

Publishing type：Research paper (scientific journal)   Publisher：Elsevier BV  

DOI： 10.1016/j.bbrc.2023.02.055

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Publishing type：Research paper (scientific journal)   Publisher：Portland Press Ltd.  

Translational elongation factor EF-Tu, which delivers aminoacyl-tRNA to the ribosome, is susceptible to inactivation by reactive oxygen species (ROS) in the cyanobacterium Synechocystis sp. PCC 6803. However, the sensitivity to ROS of chloroplast-localized EF-Tu (cpEF-Tu) of plants remains to be elucidated. In the present study, we generated a recombinant cpEF-Tu protein of Arabidopsis thaliana and examined its sensitivity to ROS in vitro. In cpEF-Tu that lacked a bound nucleotide, one of the two cysteine residues, Cys149 and Cys451, in the mature protein was sensitive to oxidation by H2O2, with the resultant formation of sulfenic acid. The translational activity of cpEF-Tu, as determined with an in vitro translation system, derived from Escherichia coli, that had been reconstituted without EF-Tu, decreased with the oxidation of a cysteine residue. Replacement of Cys149 with an alanine residue rendered cpEF-Tu insensitive to inactivation by H2O2, indicating that Cys149 might be the target of oxidation. By contrast, cpEF-Tu that had bound either GDP or GTP was less sensitive to oxidation by H2O2 than nucleotide-free cpEF-Tu. Addition of thioredoxin f1, a major thioredoxin in the Arabidopsis chloroplast, to oxidized cpEF-Tu allowed the reduction of Cys149 and the reactivation of cpEF-Tu, suggesting that the oxidation of cpEF-Tu might be a reversible regulatory mechanism that suppresses the chloroplast translation system in a redox-dependent manner.

DOI： 10.1042/bcj20220609

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：Proceedings of the National Academy of Sciences  

<jats:p>
Chloroplast F
<jats:sub>o</jats:sub>
F
<jats:sub>1</jats:sub>
-ATP synthase (CF
<jats:sub>o</jats:sub>
CF
<jats:sub>1</jats:sub>
) converts proton motive force into chemical energy during photosynthesis. Although many studies have been done to elucidate the catalytic reaction and its regulatory mechanisms, biochemical analyses using the CF
<jats:sub>o</jats:sub>
CF
<jats:sub>1</jats:sub>
complex have been limited because of various technical barriers, such as the difficulty in generating mutants and a low purification efficiency from spinach chloroplasts. By taking advantage of the powerful genetics available in the unicellular green alga
<jats:italic>Chlamydomonas reinhardtii</jats:italic>
, we analyzed the ATP synthesis reaction and its regulation in CF
<jats:sub>o</jats:sub>
CF
<jats:sub>1</jats:sub>
. The domains in the γ subunit involved in the redox regulation of CF
<jats:sub>o</jats:sub>
CF
<jats:sub>1</jats:sub>
were mutated based on the reported structure. An in vivo analysis of strains harboring these mutations revealed the structural determinants of the redox response during the light/dark transitions. In addition, we established a half day purification method for the entire CF
<jats:sub>o</jats:sub>
CF
<jats:sub>1</jats:sub>
complex from
<jats:italic>C. reinhardtii</jats:italic>
and subsequently examined ATP synthesis activity by the acid–base transition method. We found that truncation of the β-hairpin domain resulted in a loss of redox regulation of ATP synthesis (i.e., constitutively active state) despite retaining redox-sensitive Cys residues. In contrast, truncation of the redox loop domain containing the Cys residues resulted in a marked decrease in the activity. Based on this mutation analysis, we propose a model of redox regulation of the ATP synthesis reaction by the cooperative function of the β-hairpin and the redox loop domains specific to CF
<jats:sub>o</jats:sub>
CF
<jats:sub>1</jats:sub>
.
</jats:p>

DOI： 10.1073/pnas.2218187120

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Publishing type：Research paper (scientific journal)   Publisher：Elsevier BV  

DOI： 10.1016/j.jbc.2022.102650

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DOI： 10.1016/j.jbc.2022.102541

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Phosphoribulokinase (PRK), one of the enzymes in the Calvin-Benson cycle, is a well-known target of thioredoxin (Trx), which regulates various enzyme activities by the reduction of disulfide bonds in a light-dependent manner. PRK has two Cys pairs conserved in the N-terminal and C-terminal regions, and the N-terminal one near the active site is thought to be responsible for the regulation. The flexible clamp loop located between the N-terminal two Cys residues has been deemed significant to Trx-mediated regulation. However, cyanobacterial PRK is also subject to Trx-dependent activation despite the lack of this clamp loop. We, therefore, compared Trx-mediated regulation of PRK from the cyanobacterium Anabaena sp. PCC 7120 (A.7120_PRK) and that from the land plant Arabidopsis thaliana (AtPRK). Interestingly, peptide mapping and site-directed mutagenesis analysis showed that Trx was more effective in changing the redox states of the C-terminal Cys pair in both A.7120_PRK and AtPRK. In addition, the effect of redox state change of the C-terminal Cys pair on PRK activity was different between A.7120_PRK and AtPRK. Trx-mediated redox regulation of the C-terminal Cys pair was also important for complex dissociation/formation with CP12 and glyceraldehyde 3-phosphate dehydrogenase. Furthermore, in vivo analysis of the redox states of PRK showed that only one disulfide bond is reduced in response to light. Based on the enzyme activity assay and the complex formation analysis, we concluded that Trx-mediated regulation of the C-terminal Cys pair of PRK is important for activity regulation in cyanobacteria and complex dissociation/formation in both organisms.

DOI： 10.1093/pcp/pcac050

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Thioredoxin (Trx) is a key protein of the redox regulation system in chloroplasts, where it modulates various enzyme activities. Upon light irradiation, Trx reduces the disulfide bonds of Trx target proteins (thereby turning on their activities) using reducing equivalents obtained from the photosynthetic electron transport chain. This reduction process involves a differential response, i.e., some Trx target proteins in the stroma respond slowly to the change in redox condition caused by light/dark changes, while the ATP synthase γ subunit (CF1-γ) located on the surface of thylakoid membrane responds with high sensitivity. The factors that determine this difference in redox kinetics are not yet known, although here, we hypothesize that it is due to each protein's localization in the chloroplast, i.e., the reducing equivalents generated under light conditions can be transferred more efficiently to the proteins on thylakoid membrane than to stromal proteins. To explore this possibility, we anchored SBPase, one of the stromal Trx target proteins, to the thylakoid membrane in Arabidopsis thaliana. Analyses of the redox behaviors of the anchored and unanchored proteins showed no significant difference in their reduction kinetics, implying that protein sensitivity to redox regulation is determined by other factors.

DOI： 10.3390/antiox11040773

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Thioredoxin (Trx) is a protein that mediates the reducing power transfer from the photosynthetic electron transport system to target enzymes in chloroplasts and regulates their activities. Redox regulation governed by Trx is a system that is central to the adaptation of various chloroplast functions to the ever-changing light environment. However, the factors involved in the opposite reaction (i.e., the oxidation of various enzymes) have yet to be revealed. Recently, it has been suggested that Trx and Trx-like proteins could oxidize Trx-targeted proteins in vitro. To elucidate the in vivo function of these proteins as oxidation factors, we generated mutant plant lines deficient in Trx or Trx-like proteins and studied how the proteins are involved in oxidative regulation in chloroplasts. We found that f-type Trx and two types of Trx-like proteins, Trx-like 2 and atypical Cys His-rich Trx (ACHT), seemed to serve as oxidation factors for Trx-targeted proteins, such as fructose-1,6-bisphosphatase, Rubisco activase, and the γ-subunit of ATP synthase. In addition, ACHT was found to be involved in regulating nonphotochemical quenching, which is the mechanism underlying the thermal dissipation of excess light energy. Overall, these results indicate that Trx and Trx-like proteins regulate chloroplast functions in concert by controlling the redox state of various photosynthesis-related proteins in vivo.

DOI： 10.1073/pnas.2114952118

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DOI： 10.1016/j.jbc.2021.101027

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Many enzymes involved in photosynthesis possess highly conserved cysteine residues that serve as redox switches in chloroplasts. These redox switches function to activate or deactivate enzymes during light-dark transitions and have the function of fine-tuning their activities according to the intensity of light. Accordingly, many studies on chloroplast redox regulation have been conducted under the hypothesis that "fine regulation of the activities of these enzymes is crucial for efficient photosynthesis." However, the impact of the regulatory system on plant metabolism is still unclear. To test this hypothesis, we here studied the impact of the ablation of a redox switch in chloroplast NADP-malate dehydrogenase (MDH). By genome editing, we generated a mutant plant whose MDH lacks one of its redox switches and is active even in dark conditions. Although NADPH consumption by MDH in the dark is expected to be harmful to plant growth, the mutant line did not show any phenotypic differences under standard long-day conditions. In contrast, the mutant line showed severe growth retardation under short-day or fluctuating light conditions. These results indicate that thiol-switch redox regulation of MDH activity is crucial for maintaining NADPH homeostasis in chloroplasts under these conditions.

DOI： 10.1073/pnas.2016903118

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Various proteins in plant chloroplasts are subject to thiol-based redox regulation, allowing light-responsive control of chloroplast functions. Most redox-regulated proteins are known to be reductively activated in the light in a thioredoxin (Trx)-dependent manner, but its regulatory network remains incompletely understood. Using a biochemical procedure, we here show that a specific form of phosphofructokinase (PFK) is a novel redox-regulated protein whose activity is suppressed upon the reduction. PFK is a key enzyme in the glycolytic pathway. In Arabidopsis thaliana, PFK5 is targeted to chloroplasts and uniquely contains an insertion sequence harboring two Cys residues (Cys152 and Cys157) in the N-terminal region. Redox shift assays using a thiol-modifying reagent indicated that PFK5 is efficiently reduced by a specific type of Trx, namely, Trx-f. PFK5 enzyme activity was lowered with the Trx-f-dependent reduction. PFK5 redox regulation was bidirectional; PFK5 was also oxidized and activated by the recently identified Trx-like2/2-Cys peroxiredoxin pathway. Mass spectrometry-based peptide mapping analysis revealed that Cys152 and Cys157 are critical for the intramolecular disulfide bond formation in PFK5. The involvement of Cys152 and Cys157 in PFK5 redox regulation was further supported by a site-directed mutagenesis study. PFK5 catalyzes the reverse reaction of fructose 1,6-bisphosphatase (FBPase), which is reduced and activated specifically by Trx-f. Our data suggest that PFK5 redox regulation, together with that of FBPase, constitutes a checkpoint for switching light/dark metabolism in chloroplasts.

DOI： 10.1093/pcp/pcaa174

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Photosynthetic electron transport occurs on the thylakoid membrane of chloroplasts. Ferredoxin (Fd), the final acceptor in the electron transport chain, distributes electrons to several Fd-dependent enzymes including Fd-thioredoxin reductase (FTR). A cascade from Fd to FTR further reduces Thioredoxin (Trx), which tunes the activity of target metabolic enzymes eventually in a light-dependent manner. We previously reported that 10 Trx isoforms in Arabidopsis thaliana can be clustered into three classes based on the kinetics of the FTR-dependent reduction (high-, middle-, and low-efficiency classes). In this study, we determined the X-ray structure of three electron transfer complexes of FTR and Trx isoform, Trx-y1, Trx-f2, and Trx-m2, as representative examples of each class. Superposition of the FTR structure with/without Trx showed no main chain structural changes upon complex formation. There was no significant conformational change for single and complexed Trx-m structures. Nonetheless, the interface of FTR:Trx complexes displayed significant variation. Comparative analysis of the three structures showed two types of intermolecular interactions; (i) common interactions shared by all three complexes and (ii) isoform-specific interactions, which might be important for fine-tuning FTR:Trx activity. Differential electrostatic potentials of Trx isoforms may be key to isoform-specific interactions.

DOI： 10.1002/pro.3964

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The activity of the molecular motor enzyme, chloroplast ATP synthase, is regulated in a redox-dependent manner. The γ subunit, CF1-γ, is the central shaft of this enzyme complex and possesses the redox-active cysteine pair, which is reduced by thioredoxin (Trx). In light conditions, Trx transfers the reducing equivalent obtained from the photosynthetic electron transfer system to the CF1-γ. Previous studies showed that the light-dependent reduction of CF1-γ is more rapid than those of other Trx target proteins in the stroma. Although there are multiple Trx isoforms in chloroplasts, it is not well understood as to which chloroplast Trx isoform primarily contributes to the reduction of CF1-γ, especially under physiological conditions. We therefore performed direct assessment of the CF1-γ reduction capacity of each of the Trx isoforms. The kinetic analysis of the reduction process showed no significant difference in the reduction efficiency between two major chloroplast Trxs, namely Trx-f and Trx-m. Based on the thorough analyses of the CF1-γ redox dynamics in Arabidopsis thaliana Trx mutant plants, we found that lack of Trx-f or Trx-m had no significant impact on the in vivo light-dependent reduction of CF1-γ. The results showed that CF1-γ can accept the reducing power from both Trx-f and Trx-m in chloroplasts.

DOI： 10.1016/j.bbabio.2020.148261

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Thiol-based redox regulation is a post-translational protein modification for controlling enzyme activity by switching oxidation/reduction states of Cys residues. In plant cells, numerous proteins involved in a wide range of biological systems have been suggested as the target of redox regulation; however, our knowledge on this issue is still incomplete. Here we report that 3-phosphoglycerate dehydrogenase (PGDH) is a novel redox-regulated protein. PGDH catalyzes the first committed step of Ser biosynthetic pathway in plastids. Using an affinity chromatography-based method, we found that PGDH physically interacts with thioredoxin (Trx), a key factor of redox regulation. The in vitro studies using recombinant proteins from Arabidopsis thaliana showed that a specific PGDH isoform, PGDH1, forms the intramolecular disulfide bond under nonreducing conditions, which lowers PGDH enzyme activity. MS and site-directed mutagenesis analyses allowed us to identify the redox-active Cys pair that is mainly involved in disulfide bond formation in PGDH1; this Cys pair is uniquely found in land plant PGDH. Furthermore, we revealed that some plastidial Trx subtypes support the reductive activation of PGDH1. The present data show previously uncharacterized regulatory mechanisms of PGDH and expand our understanding of the Trx-mediated redox-regulatory network in plants.

DOI： 10.1074/jbc.RA120.014263

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DOI： 10.1016/j.tet.2020.131387

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In the nitrogen-fixing cyanobacterium Anabaena sp. PCC 7120, glucose 6-phosphate dehydrogenase (G6PDH) plays an important role in producing the power for reducing nitrogenase under light conditions. Our previous study showed that thioredoxin suppresses G6PDH by reducing its activator protein OpcA, implying that G6PDH is inactivated under light conditions because thioredoxins are reduced by the photosynthetic electron transport system in cyanobacteria. To address how Anabaena sp. PCC 7120 maintains G6PDH activity even under light conditions when nitrogen fixation occurs, we investigated the redox regulation system in vegetative cells and specific nitrogen-fixing cells named heterocysts, individually. We found that thioredoxin target proteins were more oxidized in heterocysts than in vegetative cells under light conditions. Alterations in the redox regulation mechanism of heterocysts may affect the redox states of thioredoxin target proteins, including OpcA, so that G6PDH is activated in heterocysts even under light conditions.

DOI： 10.1093/jxb/erz561

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DOI： 10.1074/jbc.RA119.010401

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DOI： 10.3389/fpls.2019.01534

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DOI： 10.3390/antiox7110153

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DOI： 10.1111/tpj.14000

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DOI： 10.1073/pnas.1808284115

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Language：English   Publishing type：Research paper (scientific journal)   Publisher：Portland Press Ltd  

DOI： 10.1042/BCJ20170869

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DOI： 10.1042/BCJ20161089

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In Arabidopsis thaliana, small interfering RNAs (siRNAs) generated by two Dicer isoforms, DCL3 and DCL4, function in distinct epigenetic processes, i.e. RNA-directed DNA methylation and post-transcriptional gene silencing, respectively. Plants often respond to their environment by producing a distinct set of small RNAs; however, the mechanism for controlling the production of different siRNAs from the same dsRNA substrate remains unclear. We established a simple biochemical method to visualize the dsRNA-cleaving activities of DCL3 and DCL4 in cell-free extracts prepared from Arabidopsis seedlings. Here, we demonstrate that different nutrient statuses of a host plant affect the post-translational regulation of the dicing activity of DCL3 and DCL4. Phosphate deficiency inhibited DCL3, and the activity of DCL3 was directly activated by inorganic phosphate. Sulfur deficiency inhibited DCL4 but not DCL3, and the activity of DCL4 was recovered by supplementation of the cell-free extracts with reductants containing a thiol group. Immunopurified DCL4 was activated by recombinant Arabidopsis thioredoxin-h1 with dithiothreitol. Therefore, DCL4 is subject to redox regulation. These results demonstrate that post-translational regulation of DCL activities fine-tunes the balance between branches of the gene silencing pathway according to the growth environment.

DOI： 10.1093/pcp/pcw226

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DOI： 10.1093/pcp/pcw182

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Language：Japanese   Publisher：Japanese Biochemical Society  

DOI： 10.14952/SEIKAGAKU.2017.890432

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DOI： 10.1073/pnas.1604101113

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DOI： 10.1074/jbc.M115.706424

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Language：Japanese   Publisher：The Japanese Society of Photosynthesis Research  

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DOI： 10.1074/jbc.M115.647545

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DOI： 10.1093/pcp/pcu066

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DOI： 10.1111/j.1365-3040.2011.02384.x

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DOI： 10.4161/psb.6.6.15224

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DOI： 10.1111/j.1365-3040.2010.02267.x

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DOI： 10.1016/j.mito.2007.09.003

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