Chloroplasts require glutathione reductase to balance reactive oxygen species and maintain efficient photosynthesis

• Published in: The Plant journal : for cell and molecular biology Vol. 103; no. 3; pp. 1140 - 1154
• Main Authors: Müller‐Schüssele, Stefanie J., Wang, Ren, Gütle, Desirée D., Romer, Jill, Rodriguez‐Franco, Marta, Scholz, Martin, Buchert, Felix, Lüth, Volker M., Kopriva, Stanislav, Dörmann, Peter, Schwarzländer, Markus, Reski, Ralf, Hippler, Michael, Meyer, Andreas J.
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.08.2020
• Subjects: antheraxanthin; Arabidopsis - enzymology; Arabidopsis - metabolism; Arabidopsis - physiology; Arabidopsis Proteins - metabolism; Arabidopsis Proteins - physiology; Arabidopsis thaliana; Ascorbic acid; Bryopsida - enzymology; Bryopsida - metabolism; Bryopsida - physiology; Cell Cycle Proteins - metabolism; Cell Cycle Proteins - physiology; chloroplast; chloroplast proteins; Chloroplasts; Chloroplasts - enzymology; Chloroplasts - metabolism; Chloroplasts - physiology; Detoxification; Embryos; Gene Knockout Techniques; Glutathione; Glutathione - metabolism; glutathione redox potential; Glutathione reductase; Glutathione Reductase - metabolism; Glutathione Reductase - physiology; glutathione-disulfide reductase; Homology; Labeling; lighting; Luminous intensity; Metabolism; Mitochondria; moss; mosses and liverworts; Mutants; non‐photochemical quenching; Oxidation; Oxidation-Reduction; Photosynthesis; Physcomitrella patens; Plant growth; Proteins; Reactive oxygen species; Reactive Oxygen Species - metabolism; Redox potential; redox‐sensitive GFP; Reductases; Thioredoxin; thioredoxins; Zeaxanthin; moss; non-photochemical quenching; redox-sensitive GFP; chloroplast; photosynthesis; Physcomitrella patens; reactive oxygen species; glutathione redox potential; glutathione reductase
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.14791

Summary Thiol‐based redox‐regulation is vital for coordinating chloroplast functions depending on illumination and has been throroughly investigated for thioredoxin‐dependent processes. In parallel, glutathione reductase (GR) maintains a highly reduced glutathione pool, enabling glutathione‐mediated redox buffering. Yet, how the redox cascades of the thioredoxin and glutathione redox machineries integrate metabolic regulation and detoxification of reactive oxygen species remains largely unresolved because null mutants of plastid/mitochondrial GR are embryo‐lethal in Arabidopsis thaliana. To investigate whether maintaining a highly reducing stromal glutathione redox potential (EGSH) via GR is necessary for functional photosynthesis and plant growth, we created knockout lines of the homologous enzyme in the model moss Physcomitrella patens. In these viable mutant lines, we found decreasing photosynthetic performance and plant growth with increasing light intensities, whereas ascorbate and zeaxanthin/antheraxanthin levels were elevated. By in vivo monitoring stromal EGSH dynamics, we show that stromal EGSH is highly reducing in wild‐type and clearly responsive to light, whereas an absence of GR leads to a partial glutathione oxidation, which is not rescued by light. By metabolic labelling, we reveal changing protein abundances in the GR knockout plants, pinpointing the adjustment of chloroplast proteostasis and the induction of plastid protein repair and degradation machineries. Our results indicate that the plastid thioredoxin system is not a functional backup for the plastid glutathione redox systems, whereas GR plays a critical role in maintaining efficient photosynthesis. Significance Statement Chloroplast physiology in the light and in the dark is underpinned by various redox cascades, modulating scavenging of reactive oxygen species, damage repair and enzymatic functions. We find that the glutathione redox potential (EGSH) dynamically reacts to light and that a permanently shifted EGSH causes light‐sensitivity, disturbing non‐photochemical quenching and protein homeostasis. Our data suggest that redox processes downstream of stromal EGSH play a fundamental role in regulating photosynthetic efficiency.