Putative role of the malate valve enzyme NADP–malate dehydrogenase in H ₂ O ₂ signalling in Arabidopsis

Abstract

In photosynthetic organisms, sudden changes in light intensity perturb the photosynthetic electron flow and lead to an increased production of reactive oxygen species. At the same time, thioredoxins can sense the redox state of the chloroplast. According to our hypothesis, thioredoxins and related thiol reactive molecules downregulate the activity of H 2 O 2 -detoxifying enzymes, and thereby allow a transient oxidative burst that triggers the expression of H 2 O 2 responsive genes. It has been shown recently that upon light stress, catalase activity was reversibly inhibited in Chlamydomonas reinhardtii in correlation with a transient increase in the level of H 2 O 2 . Here, it is shown that Arabidopsis thaliana mutants lacking the NADP -malate dehydrogenase have lost the reversible inactivation of catalase activity and the increase in H 2 O 2 levels when exposed to high light. The mutants were slightly affected in growth and accumulated higher levels of NADPH in the chloroplast than the wild-type. We propose that the malate valve plays an essential role in the regulation of catalase activity and the accumulation of a H 2 O 2 signal by transmitting the redox state of the chloroplast to other cell compartments.

Thiol switches in redox regulation of chloroplasts: balancing redox state, metabolism and oxidative stress

“…It has been proposed that the antioxidant activity is regulated. Such mechanisms would allow for control of local signaling in macromolecular assemblies on the scale of nanometers vs. more distant signaling on the submicrometer to micrometer scale by diffusion (Heyno et al, 2014). Buffering of ROS and redox disequilibria is not only achieved by the enzymatic and non-enzymatic antioxidants, but also by the huge concentration of protein thiols, which exceeds the glutathione pool more than 10-fold (Muthuramalingam et al, 2013).…”

Redox- and Reactive Oxygen Species-Dependent Signaling into and out of the Photosynthesizing Chloroplast

“…A transient increase in H 2 O 2 levels upon light stress depends on the reversible thiol-dependent inhibition of catalase activity (Michelet et al, 2013). Mutants affected in NADP-MDH lack the transient down-regulation of catalase activity and the concomitant transient increase in H 2 O 2 levels (Heyno et al, 2014). Catalase in higher plants is localized to the peroxisome.…”

Photosynthesis under artificial light: the shift in primary and secondary metabolism

“…Some of these mechanisms are the specific topic of other papers included in this special issue (xanthophyll cycle [33], non-photochemical quenching [34], re-oxidation of the reduction equivalents through photorespiration, the malate valve and the action of antioxidants [35]). This section is dedicated to the metabolic shifts triggered by high light stress.…”