A Failure Mode and Effect Analysis of plant metabolism reveals why
cytosolic fumarase is required for temperature acclimation in
Arabidopsis
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 is currently unclear. 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
acclimation not only to low temperatures, as previously shown, but also
to increased temperature. To understand the role of FUM2 activity, we
have adapted a reliability engineering technique, Failure Mode and
Effect Analysis (FMEA), to apply it to a biological problem. This allows
us to formalize a rigorous approach for ranking metabolites according to
the potential risk they pose to the metabolic system. FMEA identifies
fumarate as a low-risk metabolite. 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, maintaining
system stability under changing environmental conditions.