Metabolic flux from the chloroplast provides signals controlling photosynthetic acclimation to cold in Arabidopsis thaliana.

Helena A Herrmann,Beth C Dyson,Matthew A E Miller,Jean‐Marc Schwartz,Giles N Johnson

doi:10.1111/pce.13896

Abstract

Photosynthesis is especially sensitive to environmental conditions, and the composition of the photosynthetic apparatus can be modulated in response to environmental change, a process termed photosynthetic acclimation. Previously, we identified a role for a cytosolic fumarase, FUM2 in acclimation to low temperature in Arabidopsis thaliana. Mutant lines lacking FUM2 were unable to acclimate their photosynthetic apparatus to cold. Here, using gas exchange measurements and metabolite assays of acclimating and non-acclimating plants, we show that acclimation to low temperature results in a change in the distribution of photosynthetically fixed carbon to different storage pools during the day. Proteomic analysis of wild-type Col-0 Arabidopsis and of a fum2 mutant, which was unable to acclimate to cold, indicates that extensive changes occurring in response to cold are affected in the mutant. Metabolic and proteomic data were used to parameterize metabolic models. Using an approach called flux sampling, we show how the relative export of triose phosphate and 3-phosphoglycerate provides a signal of the chloroplast redox state that could underlie photosynthetic acclimation to cold.

Highlights

Through their lifecycle, plants experience environmental conditions that vary on timescales from seconds to seasons
Previous work has shown that the ability to acclimate photosynthesis and metabolism to changes in light plays an important role in determining plant fitness and seed yield (Athanasiou et al, 2010)
We have presented evidence that acclimation to cold is important in determining fitness and seed yield – wild-type Col-0 plants are unaffected by changes in temperature, while fum2.2, which is unable to acclimate to cold, is negatively affected by even short cold periods

Summary

| INTRODUCTION

Plants experience environmental conditions that vary on timescales from seconds to seasons. Limitations in flux through sucrose phosphate synthase (SPS) result in the accumulation of phosphorylated metabolites (Hurry, Strand, Furbank, & Stitt, 2000) This is thought to lead to depletion of the cytosolic concentration of inorganic phosphate (Pi), which, in turn, limits the export of triose phosphate (TP) from the chloroplast. While wild-type Col-0 Arabidopsis plants increase photosynthetic capacity in response to low temperature, fum mutant plants do not This suggests that Pi deficiency alone is not sufficient to trigger photosynthetic acclimation. Based on the results from metabolic modelling, constrained using experimental data, we propose that the changes in the pathway of carbohydrate export from the chloroplast link to fumarate accumulation at low temperature and provide a mechanism controlling photosynthetic acclimation to cold

| MATERIALS AND METHODS

| RESULTS

Findings

| DISCUSSION