Self-protection of cytosolic malate dehydrogenase against oxidative stress in Arabidopsis

Huang, Jingjing; Niazi, Adnan; Young, Diana; Rosado, Leonardo Astolfi; Vertommen, Didier; Bodra, Nandita; Gawwad, Mohamed Ragab Abdel; Vignols, Florence; Wei, Bo; Wahni, Khadija; Bashandy, Talaat; Bariat, Laetitia; Breusegem, Frank Van; Messens, Joris; Reichheld, Jean‐Philippe

doi:10.1093/jxb/erx396

Cited by 54 publications

(43 citation statements)

References 53 publications

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“…Reduced AtMAPK4 proteins (20 μM) were incubated with 2 mM dimedone. For AtMAPK4 oxidation, 1 mM H 2 O 2 was incubated at room temperature for 1 h. The in vitro dimedone labeling and detection by Western blot and LC-MS/MS were as described previously, with adaptations (68). For additional information, see SI Appendix, Materials and Methods.…”

Section: Methodsmentioning

confidence: 99%

Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites

Huang

Willems

Wei

et al. 2019

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

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Hydrogen peroxide (H2O2) is an important messenger molecule for diverse cellular processes. H2O2 oxidizes proteinaceous cysteinyl thiols to sulfenic acid, also known as S-sulfenylation, thereby affecting the protein conformation and functionality. Although many proteins have been identified as S-sulfenylation targets in plants, site-specific mapping and quantification remain largely unexplored. By means of a peptide-centric chemoproteomics approach, we mapped 1,537 S-sulfenylated sites on more than 1,000 proteins in Arabidopsis thaliana cells. Proteins involved in RNA homeostasis and metabolism were identified as hotspots for S-sulfenylation. Moreover, S-sulfenylation frequently occurred on cysteines located at catalytic sites of enzymes or on cysteines involved in metal binding, hinting at a direct mode of action for redox regulation. Comparison of human and Arabidopsis S-sulfenylation datasets provided 155 conserved S-sulfenylated cysteines, including Cys181 of the Arabidopsis MITOGEN-ACTIVATED PROTEIN KINASE4 (AtMAPK4) that corresponds to Cys161 in the human MAPK1, which has been identified previously as being S-sulfenylated. We show that, by replacing Cys181 of recombinant AtMAPK4 by a redox-insensitive serine residue, the kinase activity decreased, indicating the importance of this noncatalytic cysteine for the kinase mechanism. Altogether, we quantitatively mapped the S-sulfenylated cysteines in Arabidopsis cells under H2O2 stress and thereby generated a comprehensive view on the S-sulfenylation landscape that will facilitate downstream plant redox studies.

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Section: Methodsmentioning

confidence: 99%

Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites

Huang

Willems

Wei

et al. 2019

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

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124

115

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“…Apparently, this isoform is sensitive to H 2 O 2 through sulphur oxidation of cysteines and methionines affecting its kinetics, secondary structure and thermodynamic stability. Furthermore, the reversible homodimerisation and reduction of cyNAD-MDH 1 protects the protein from overoxidation (Huang et al 2018).…”

Section: Cytosolic Mdhs Mediate Intercompartmental Energy Exchangementioning

confidence: 99%

“…Furthermore, the reversible homodimerisation and reduction of cyNAD‐MDH 1 protects the protein from over‐oxidation (Huang et al . ).…”

Section: Introductionmentioning

confidence: 97%

Malate valves: old shuttles with new perspectives

2018

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Malate valves act as powerful systems for balancing the ATP/NAD(P)H ratio required in various subcellular compartments in plant cells. As components of malate valves, isoforms of malate dehydrogenases (MDHs) and dicarboxylate translocators catalyse the reversible interconversion of malate and oxaloacetate and their transport. Depending on the co-enzyme specificity of the MDH isoforms, either NADH or NADPH can be transported indirectly. Arabidopsis thaliana possesses nine genes encoding MDH isoenzymes. Activities of NAD-dependent MDHs have been detected in mitochondria, peroxisomes, cytosol and plastids. In addition, chloroplasts possess a NADP-dependent MDH isoform. The NADP-MDH as part of the 'light malate valve' plays an important role as a poising mechanism to adjust the ATP/NADPH ratio in the stroma. Its activity is strictly regulated by post-translational redox-modification mediated via the ferredoxin-thioredoxin system and fine control via the NADP /NADP(H) ratio, thereby maintaining redox homeostasis under changing conditions. In contrast, the plastid NAD-MDH ('dark malate valve') is constitutively active and its lack leads to failure in early embryo development. While redox regulation of the main cytosolic MDH isoform has been shown, knowledge about regulation of the other two cytosolic MDHs as well as NAD-MDH isoforms from peroxisomes and mitochondria is still lacking. Knockout mutants lacking the isoforms from chloroplasts, mitochondria and peroxisomes have been characterised, but not much is known about cytosolic NAD-MDH isoforms and their role in planta. This review updates the current knowledge on MDH isoforms and the shuttle systems for intercompartmental dicarboxylate exchange, focusing on the various metabolic functions of these valves.

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“…However, alternative locations were also observed for some of them, including the plasma membrane, endomembranes (endoplasmic reticulum and golgi), mitochondria, and the nucleus (Serrato & Cejudo, 2003;Traverso et al, 2013). Given the number of TRX h isoforms, the high redundancy among this gene family is not surprising (Huang et al, 2017), which makes it rather difficult to unequivocally determine the function of each TRX h isoform (Meyer et al, 2009(Meyer et al, , 2012Buchanan, 2017). This fact aside, a number of studies provided evidence that the function of these TRXs are associated with seed germination (Hägglund et al, 2016;Li et al, 2009), calcium signalling (Ueoka-Nakanishi et al, 2013), glycolysis (Piattoni, Guerrero, & Iglesias, 2013), and cell-to-cell communication (Meng et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Thioredoxin h2 contributes to the redox regulation of mitochondrial photorespiratory metabolism

Fonseca‐Pereira

Souza

Hou

et al. 2019

Plant Cell & Environment

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Thioredoxins (TRXs) are important proteins involved in redox regulation of metabolism. In plants, it has been shown that the mitochondrial metabolism is regulated by the mitochondrial TRX system. However, the functional significance of TRX h2, which is found at both cytosol and mitochondria, remains unclear. Arabidopsis plants lacking TRX h2 showed delayed seed germination and reduced respiration alongside impaired stomatal and mesophyll conductance, without impacting photosynthesis under ambient O2 conditions. However, an increase in the stoichiometry of photorespiratory CO2 release was found during O2‐dependent gas exchange measurements in trxh2 mutants. Metabolite profiling of trxh2 leaves revealed alterations in key metabolites of photorespiration and in several metabolites involved in respiration and amino acid metabolism. Decreased abundance of serine hydroxymethyltransferase and glycine decarboxylase (GDC) H and L subunits as well as reduced NADH/NAD+ ratios were also observed in trxh2 mutants. We further demonstrated that the redox status of GDC‐L is altered in trxh2 mutants in vivo and that recombinant TRX h2 can deactivate GDC‐L in vitro, indicating that this protein is redox regulated by the TRX system. Collectively, our results demonstrate that TRX h2 plays an important role in the redox regulation of mitochondrial photorespiratory metabolism.

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Self-protection of cytosolic malate dehydrogenase against oxidative stress in Arabidopsis

Cited by 54 publications

References 53 publications

Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites

Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites

Malate valves: old shuttles with new perspectives

Thioredoxin h2 contributes to the redox regulation of mitochondrial photorespiratory metabolism

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