Thioredoxin and Glutaredoxin Systems in Plants: Molecular Mechanisms, Crosstalks, and Functional Significance

Thioredoxins (Trx) and glutaredoxins (Grx) constitute families of thiol oxidoreductases. Our knowledge of Trx and Grx in plants has dramatically increased during the last decade. The release of the Arabidopsis genome sequence revealed an unexpectedly high number of Trx and Grx genes. The availability of several genomes of vascular and nonvascular plants allowed the establishment of a clear classification of the genes and the chronology of their appearance during plant evolution. Proteomic approaches have been developed that identified the putative Trx and Grx target proteins which are implicated in all aspects of plant growth, including basal metabolism, iron/sulfur cluster formation, development, adaptation to the environment, and stress responses. Analyses of the biochemical characteristics of specific Trx and Grx point to a strong specificity toward some target enzymes, particularly within plastidial Trx and Grx. In apparent contradiction with this specificity, genetic approaches show an absence of phenotype for most available Trx and Grx mutants, suggesting that redundancies also exist between Trx and Grx members. Despite this, the isolation of mutants inactivated in multiple genes and several genetic screens allowed the demonstration of the involvement of Trx and Grx in pathogen response, phytohormone pathways, and at several control points of plant development. Cytosolic Trxs are reduced by NADPH-thioredoxin reductase (NTR), while the reduction of Grx depends on reduced glutathione (GSH). Interestingly, recent development integrating biochemical analysis, proteomic data, and genetics have revealed an extensive crosstalk between the cytosolic NTR/Trx and GSH/Grx systems. This crosstalk, which occurs at multiple levels, reveals the high plasticity of the redox systems in plants. Antioxid. Redox Signal. 00, 000–000. I. Introduction II. Peptidyl Cysteine Oxidation and Reduction by Trx and Grx A. Reduction of disulfide bridges and sulfenic acids B. S-glutathionylation/deglutathionylation and isomerization C. S-nitrosylation/denitrosylation III. Trx-Dependent Reduction System in Plants A. Trx reduction B. Trx and putative target proteins 1. Plastidial Trx a. Metabolic and antioxidant functions b. New functions of chloroplastic Trx c. Atypical chloroplastic Trx 2. Mitochondrial Trx 3. Cytosolic and nuclear Trx IV. Grx-Dependent Reduction System in Plants A. Glutathione: synthesis, reduction, and compartmentation B. Grx and putative target proteins 1. Subgroup I: C[P/G/S]Y[C/S] Grx 2. Subgroup II: CGFS Grx 3. Subgroup III: CCx[C/S/G] or ROXY Grx 4. Subgroup IV: 4CxxC Grx 5. Subgroup V: CPF[C/S] Grx V. Isolation of Trx and Grx Targets VI. The Reduction Pathway of Cytosolic and Mitochondrial Trx, Grx, and GSH Revisited A. Trx reduction by Grx B. GSSG reduction by Trx C. Atypical types of reduction VII. Genetic Evidence for Interactions Between Grx and Trx Pathways A. Genetic crosstalk between Trx and Grx systems in yeast B. Genetic crosstalk reveals new functions of Trx and Grx systems in plant development VIII. Conclusions