Singlet oxygen-induced signalling depends on the metabolic status of the Chlamydomonas cell

Abstract

Singlet oxygen (1O2) induces retrograde signalling in chloroplasts. Using a novel mutant screen, we identified a mutation in the TREHALOSE-6-PHOSPHATE PHOSPHATASE 1 (T6PP1) gene that results in accumulation of trehalose 6-phosphate, a reprogramming of cell metabolism, and impairment of 1O2-induced retrograde signalling in Chlamydomonas reinhardtii. From transcriptomic analysis and metabolite profiling, we conclude that accumulation or deficiency of certain metabolites directly affect 1O2-signalling. 1O2-inducible GLUTATHIONE PEROXIDASE 5 (GPX5) gene expression is suppressed by increased content of fumarate, an intermediate in the tricarboxylic acid cycle (TCA cycle) in mitochondria and dicarboxylate metabolism in the cytosol, while it is promoted by another TCA cycle intermediate, aconitate. Furthermore, genes encoding known essential components of chloroplast-to-nucleus 1O2-signalling show decreased transcript levels in a t6pp1 mutant, which can be rescued by exogenous application of aconitate. We demonstrate that chloroplast retrograde signalling involving 1O2 depends on mitochondrial and cytosolic processes and that the metabolic status of the cell determines the response to 1O2.