2-cysteine peroxiredoxins and thylakoid ascorbate peroxidase create a water-water cycle that is essential to protect the photosynthetic apparatus under high light stress conditions

• Published in: Plant physiology (Bethesda) Vol. 167; no. 4; pp. 1592 - 1603
• Main Authors: Awad, Jasmin, Stotz, Henrik U, Fekete, Agnes, Krischke, Markus, Engert, Cornelia, Havaux, Michel, Berger, Susanne, Mueller, Martin J
• Format: Journal Article
• Language: English
• Published: United States 01.04.2015
• Subjects: Arabidopsis - genetics; Arabidopsis - physiology; Arabidopsis - radiation effects; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Ascorbate Peroxidases - genetics; Ascorbate Peroxidases - metabolism; Carbon Dioxide - metabolism; Cysteine - metabolism; Gene Expression Regulation, Plant; Hydrogen Peroxide - metabolism; Light - adverse effects; Models, Biological; Mutation; Oxidative Stress; Peroxiredoxins - metabolism; Photosynthesis - radiation effects; Plant Leaves - genetics; Plant Leaves - physiology; Plant Leaves - radiation effects; Plants, Genetically Modified; Plastids - metabolism; Seedlings - genetics; Seedlings - physiology; Seedlings - radiation effects; Stress, Physiological; Thylakoids - enzymology; Water - physiology
• ISSN: 1532-2548; 1532-2548
• DOI: 10.1104/pp.114.255356

Different peroxidases, including 2-cysteine (2-Cys) peroxiredoxins (PRXs) and thylakoid ascorbate peroxidase (tAPX), have been proposed to be involved in the water-water cycle (WWC) and hydrogen peroxide (H2O2)-mediated signaling in plastids. We generated an Arabidopsis (Arabidopsis thaliana) double-mutant line deficient in the two plastid 2-Cys PRXs (2-Cys PRX A and B, 2cpa 2cpb) and a triple mutant deficient in 2-Cys PRXs and tAPX (2cpa 2cpb tapx). In contrast to wild-type and tapx single-knockout plants, 2cpa 2cpb double-knockout plants showed an impairment of photosynthetic efficiency and became photobleached under high light (HL) growth conditions. In addition, double-mutant plants also generated elevated levels of superoxide anion radicals, H2O2, and carbonylated proteins but lacked anthocyanin accumulation under HL stress conditions. Under HL conditions, 2-Cys PRXs seem to be essential in maintaining the WWC, whereas tAPX is dispensable. By comparison, this HL-sensitive phenotype was more severe in 2cpa 2cpb tapx triple-mutant plants, indicating that tAPX partially compensates for the loss of functional 2-Cys PRXs by mutation or inactivation by overoxidation. In response to HL, H2O2- and photooxidative stress-responsive marker genes were found to be dramatically up-regulated in 2cpa 2cpb tapx but not 2cpa 2cpb mutant plants, suggesting that HL-induced plastid to nucleus retrograde photooxidative stress signaling takes place after loss or inactivation of the WWC enzymes 2-Cys PRX A, 2-Cys PRX B, and tAPX.