Arabidopsis glutathione reductase 2 is indispensable in plastids, while mitochondrial glutathione is safeguarded by additional reduction and transport systems

• Published in: The New phytologist Vol. 224; no. 4; pp. 1569 - 1584
• Main Authors: Marty, Laurent, Bausewein, Daniela, Müller, Christopher, Bangash, Sajid Ali Khan, Moseler, Anna, Schwarzländer, Markus, Müller-Schüssele, Stefanie J., Zechmann, Bernd, Riondet, Christophe, Balk, Janneke, Wirtz, Markus, Hell, Rüdiger, Reichheld, Jean-Philippe, Meyer, Andreas J.
• Format: Journal Article
• Language: English
• Published: England Wiley 01.12.2019; Wiley Subscription Services, Inc
• Series: New Phytologist Trust
• Subjects: ABC transporters; ABCB25; Animal embryos; antioxidant activity; Antioxidants; Arabidopsis; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; ATP; ATP-Binding Cassette Transporters - genetics; ATP-Binding Cassette Transporters - metabolism; Biogenesis; Biosensors; Complementation; Cytoplasmic organelles; Cytosol; death; dual targeting; embryo lethality; Embryos; genetic complementation; Genetic Complementation Test; Glutathione; Glutathione - metabolism; glutathione redox status; Glutathione reductase; Glutathione Reductase - genetics; Glutathione Reductase - metabolism; glutathione reductase 2; glutathione-disulfide reductase; Homeostasis; In vivo methods and tests; Labeling; Lethality; Life Sciences; Mitochondria; Mitochondria - metabolism; mutants; Mutation; NTR; Organelles; Oxidation; Oxidation-Reduction; Oxidoreductions; Plant cells; plant development; Plants, Genetically Modified; Plastids; Plastids - genetics; Plastids - metabolism; Redox potential; redox‐sensitive GFP; Reductases; Seeds - genetics; Stroma; Sulfur; Sulphur; Thioredoxin; thioredoxins; Transportation systems; Viability; redox-sensitive GFP; glutathione redox status; embryo lethality; mitochondria; dual targeting; NTR; glutathione reductase 2; ABCB25; Glutathione reductase; Mitocondria
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.16086

• A highly negative glutathione redox potential (EGSH ) is maintained in the cytosol, plastids and mitochondria of plant cells to support fundamental processes, including antioxidant defence, redox regulation and ironasulfur cluster biogenesis. Out of two glutathione reductase (GR) proteins in Arabidopsis, GR2 is predicted to be dual-targeted to plastids and mitochondria, but its differential roles in these organelles remain unclear. • We dissected the role of GR2 in organelle glutathione redox homeostasis and plant development using a combination of genetic complementation and stacked mutants, biochemical activity studies, immunogold labelling and in vivo biosensing. • Our data demonstrate that GR2 is dual-targeted to plastids and mitochondria, but embryo lethality of gr2 null mutants is caused specifically in plastids. Whereas lack of mitochondrial GR2 leads to a partially oxidised glutathione pool in the matrix, the ATP-binding cassette (ABC) transporter ATM3 and the mitochondrial thioredoxin system provide functional backup and maintain plant viability. • We identify GR2 as essential in the plastid stroma, where it counters GSSG accumulation and developmental arrest. By contrast a functional triad of GR2, ATM3 and the thioredoxin system in the mitochondria provides resilience to excessive glutathione oxidation.