Cytosolic fumarase acts as a metabolic fail-safe for both high and low temperature acclimation of Arabidopsis thaliana

Abstract

Plants acclimate their photosynthetic capacity in response to changing environmental conditions. In Arabidopsis thaliana, photosynthetic acclimation to cold requires the accumulation of the organic acid fumarate, catalysed by a cytosolic fumarase FUM2. However, the role of this accumulation is currently unknown. In this study, we use an integrated experimental and modelling approach to examine the role of FUM2 and fumarate across the physiological temperature range. Using physiological and biochemical analyses, we demonstrate that FUM2 is necessary for high as well as low temperature acclimation. We have adapted a reliability engineering technique, Failure Mode and Effect Analysis (FMEA), to formalize a rigorous approach for ranking metabolites according to the potential risk that they pose to the metabolic system. FMEA identifies fumarate as a low-risk metabolite, while its precursor, malate, is shown to be high-risk and liable to cause system instability. We conclude that the role of cytosolic fumarase, FUM2, is to provide a fail-safe, controlling malate concentration, maintaining system stability in a changing environment. We argue that FMEA is a technique that is not only useful in understanding plant metabolism but can also be used to study reliability in other systems and synthetic pathways.