The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 Gene Defines a Glutathione-Dependent Pathway Involved in Initiation and Maintenance of Cell Division during Postembryonic Root Development

Vernoux, Teva; Wilson, Robert; Seeley, Kevin A.; Reichheld, Jean‐Philippe; Muroy, Sandra E; Brown, Spencer A.; Maughan, Spencer C.; Cobbett, Christopher S.; Montagu, Marc Van; Inzé, Dirk; May, Mike; Sung, Z. Renee

doi:10.2307/3871032

Cited by 148 publications

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“…3C). Interestingly, this gene is responsible for cell division in root meristem (30). Activity of cell division in root meristem might be enhanced under nutritional deficiencies to elongate roots to capture more sulfate or nitrate ions.…”

Section: Resultsmentioning

confidence: 99%

Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana

Hirai

Yano

Goodenowe

et al. 2004

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

705

519

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Plant metabolism is a complex set of processes that produce a wide diversity of foods, woods, and medicines. With the genome sequences of Arabidopsis and rice in hands, postgenomics studies integrating all ''omics'' sciences can depict precise pictures of a whole-cellular process. Here, we present, to our knowledge, the first report of investigation for gene-to-metabolite networks regulating sulfur and nitrogen nutrition and secondary metabolism in Arabidopsis, with integration of metabolomics and transcriptomics. Transcriptome and metabolome analyses were carried out, respectively, with DNA macroarray and several chemical analytical methods, including ultra high-resolution Fourier transform-ion cyclotron MS. Mathematical analyses, including principal component analysis and batch-learning self-organizing map analysis of transcriptome and metabolome data suggested the presence of general responses to sulfur and nitrogen deficiencies. In addition, specific responses to either sulfur or nitrogen deficiency were observed in several metabolic pathways: in particular, the genes and metabolites involved in glucosinolate metabolism were shown to be coordinately modulated. Understanding such geneto-metabolite networks in primary and secondary metabolism through integration of transcriptomics and metabolomics can lead to identification of gene function and subsequent improvement of production of useful compounds in plants. P lants produce a huge array of compounds used for foods, medicines, flavors, and industrial materials. These plant metabolites are synthesized and accumulated by the networks of proteins encoded in the genome of each plant. However, even after the completion of the genome sequencing of Arabidopsis (1) and rice (2, 3), function of those genes and networks of gene-to-metabolite are largely unknown. To reveal the function of genes involved in metabolic processes and gene-to-metabolite networks, the metabolomics-based approach is regarded as a direct way (4-7). In particular, integration of comprehensive gene expression profile with targeted metabolite analysis is shown to be an innovative way for identification of gene function for specific product accumulation in plant (8) and microorganisms (9). However, to depict a whole-cellular process of metabolism, integration of comprehensive gene expression analysis (transcriptomics), and nontargeted metabolite profiling (metabolomics) is needed. Bioinformatics designed suitably for data mining helps the integration efficiently.The gene expression profiling can be achieved by DNA array analysis. For metabolomics, a nontargeted, high-throughput analytical system is required. Traditionally, GC-MS has been used to detect Ͼ300 metabolites in plant tissues (5, 6). Fourier transform-ion cyclotron MS (FT-MS) is a system for metabolome analysis in which crude plant extract is introduced by means of direct injection without prior separation of metabolites by chromatography (10). The mass resolution (Ͼ100,000) and accuracy (Ͻ1 ppm) of FT-MS is extremely high; hence, comple...

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Section: Resultsmentioning

confidence: 99%

Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana

Hirai

Yano

Goodenowe

et al. 2004

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

705

519

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“…S2) and may thus explain the altered GCL activity in planta. Furthermore, a missense mutation in the Arabidopsis GCL gene (root meristemless1, rml1) has been identified (11). It substitutes Asp 259 (Asp 250 in B. juncea) for asparagine, resulting in loss of GCL activity in vivo.…”

Section: Resultsmentioning

confidence: 99%

“…It is involved in the detoxification of xenobiotics via glutathione S-transferases (5), represents the precursor for the heavy metal ions sequestering phytochelatins (6), and serves as a major defense component against a wide range of abiotic and biotic stress factors (7). GSH can post-translationally modify proteins via glutathionylation (8,9) and may act as a signaling molecule (10,11). Notably, GSH represents a major storage and transport form of reduced sulfur in plants (12).…”

mentioning

confidence: 99%

Structural Basis for the Redox Control of Plant Glutamate Cysteine Ligase

Hothorn

Wachter

Gromes

et al. 2006

Journal of Biological Chemistry

104

163

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Glutathione (GSH) plays a crucial role in plant metabolism and stress response. The rate-limiting step in the biosynthesis of GSH is catalyzed by glutamate cysteine ligase (GCL) the activity of which is tightly regulated. The regulation of plant GCLs is poorly understood. The crystal structure of substrate-bound GCL from Brassica juncea at 2.1-Å resolution reveals a plantunique regulatory mechanism based on two intramolecular redox-sensitive disulfide bonds. Reduction of one disulfide bond allows a ␤-hairpin motif to shield the active site of B. juncea GCL, thereby preventing the access of substrates. Reduction of the second disulfide bond reversibly controls dimer to monomer transition of B. juncea GCL that is associated with a significant inactivation of the enzyme. These regulatory events provide a molecular link between high GSH levels in the plant cell and associated down-regulation of its biosynthesis. Furthermore, known mutations in the Arabidopsis GCL gene affect residues in the close proximity of the active site and thus explain the decreased GSH levels in mutant plants. In particular, the mutation in rax1-1 plants causes impaired binding of cysteine.Glutathione (GSH) is the predominant non-protein thiol compound in eukaryotic and prokaryotic cells (1). Through reversible oxidation to glutathione disulfide, it acts as a major cellular redox buffer. In the plant chloroplast GSH can reach millimolar concentrations depending on diverse external stress stimuli and on the day-night transition. Light/dark-induced changes in stromal pH further modulate the redox potential of GSH (2).In plants, GSH detoxifies reactive oxygen species via the ascorbic acid-GSH-cycle (3) and glutathione peroxidases (4). It is involved in the detoxification of xenobiotics via glutathione S-transferases (5), represents the precursor for the heavy metal ions sequestering phytochelatins (6), and serves as a major defense component against a wide range of abiotic and biotic stress factors (7). GSH can post-translationally modify proteins via glutathionylation (8, 9) and may act as a signaling molecule (10, 11). Notably, GSH represents a major storage and transport form of reduced sulfur in plants (12).The biosynthesis of GSH occurs in two sequential ATP-dependent steps. Glutamate cysteine ligase (GCL, 3 EC 6.3.2.2.) produces the reaction intermediate ␥-glutamylcysteine (Scheme 1). Glutathione synthetase (EC 6.3.2.3.) then catalyzes the addition of a glycine residue.Both enzymes are encoded by single genes in Arabidopsis, belonging to the Brassicaceae family (13-15). In this plant family GCL is localized exclusively in the plastids, whereas glutathione synthetase is found both in plastids and in the cytosol (16). Under most conditions, GCL activity is rate-limiting in plant GSH biosynthesis (17). This is highlighted by significantly reduced glutathione levels in AtGCL mutants (18,19).Plant GCL protein sequences diverge from those of nonplant eukaryotic organisms (mammals, Drosophila). Although some bacteria share low sequence homology w...

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“…These positions are occupied by cysteines in the Hahb-10 leucine zipper. root hair number, and root hair length respond to the inclusion of redox agents in the growth medium (47,48), and mutants in the enzyme ␥-glutamylcysteine synthetase, involved in the synthesis of GSH, show altered root development and reduced cell division rates (49). Root hair development establishes a link between GSH and glabra2 proteins.…”

Section: Discussionmentioning

confidence: 99%

Redox Regulation of Plant Homeodomain Transcription Factors

Tron¹,

Bertoncini²,

Chan³

et al. 2002

Journal of Biological Chemistry

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Several families of plant transcription factors contain a conserved DNA binding motif known as the homeodomain. In two of these families, named Hd-Zip and glabra2, the homeodomain is associated with a leucine zipper-like dimerization motif. A group of Hd-Zip proteins, namely Hd-ZipII, contain a set of conserved cysteines within the dimerization motif and adjacent to it. Incubation of one of these proteins, Hahb-10, in the presence of thiol-reducing agents such as dithiothreitol or reduced glutathione produced a significant increase in DNA binding. Under such conditions, the protein migrated as a monomer in non-reducing SDS-polyacrylamide gels. Under oxidizing conditions, a significant proportion of the protein migrated as dimers, suggesting the formation of intermolecular disulfide bonds. A similar behavior was observed for the glabra2 protein HAHR1, which also contains two conserved cysteines within its dimerization domain. Site-directed mutagenesis of the cysteines to serines indicated that each of them has different roles in the activation of the proteins. Purified thioredoxin was able to direct the NADPH-dependent activation of Hahb-10 and HAHR1 in the presence of thioredoxin reductase. The results suggest that redox conditions may operate to regulate the activity of these groups of plant transcription factors within plant cells.

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The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 Gene Defines a Glutathione-Dependent Pathway Involved in Initiation and Maintenance of Cell Division during Postembryonic Root Development

Cited by 148 publications

References 0 publications

Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana

Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana

Structural Basis for the Redox Control of Plant Glutamate Cysteine Ligase

Redox Regulation of Plant Homeodomain Transcription Factors

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