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

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.

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

“…In terms of temperature, photosynthesis shows different responses when plants are exposed to heat or cold, although some of their signalling pathways are shared (reviewed by Sharma et al 2020; Choudjury et al 2013). Previously, we observed that photosynthetic acclimation to cold is dependent on the presence of FUM2 activity or protein (Dyson et al, 2016; Herrmann et al 2020). Thus, with the aim of understanding further the role of FUM2 and fumarate in the photosynthetic acclimation response to temperature, we analysed how its accumulation changes across the physiological temperature range in different genotypes of Arabidopsis.…”

“…Malate and fumarate represent important diurnal carbon stores in Arabidopsis, and their accumulation tends to increase at low temperature (Dyson et al 2016; Herrmann et al 2019b; Herrmann et al 2020). The Arabidopsis ecotype C24 has previously been reported to have a reduced capacity for cytosolic fumarate synthesis, while the knockout mutant fum2 is impaired in fumarate accumulation (Riewe et al, 2016; Pracharoenwattana et al 2010).…”

“…The third major diurnal carbon store in Arabidopsis is starch (Smith and Stitt, 2007; Streb and Zeeman, 2012). We previously demonstrated that the total accumulation of malate, fumarate and starch in Col-0 and fum2 changes upon cold acclimation (Dyson et al 2016, Herrmann et al 2019c, Herrmann et al 2020). We measured starch accumulation at the lowest and highest temperatures and observe the same trend, with the addition of the C24 accession (Supplementary Figure S3).…”

“…Fumarate accumulation could either act as a signal for acclimation itself or could modulate metabolic or redox responses to temperature (Dyson et al 2016; Herrmann et al 2020). If the first hypothesis were correct, we would expect similar changes in fumarate concentration to trigger similar outcomes for photosynthetic acclimation.…”

The Eucalyptus grandis chloroplast proteome: leaf development and seasonal variations

“…As chloroplasts are very sensitive to environmental fluctuations, dynamic proteome changes may represent a key factor for understanding their responses to abiotic stresses [11]. The most recent chloroplast proteomics studieshave aimed to identify (1) changes induced by biotic and abiotic stresses [12][13][14][15][16], (2) mechanisms of remodeling and reprogramming of plant metabolism [17,18], (3) biogenesis and senescence [19][20][21], (4) chloroplast development [22,23],in addition to (5) novel techniques for increasing proteome coverage [24][25][26].…”