FUM2, a Cytosolic Fumarase, Is Essential for Acclimation to Low Temperature in Arabidopsis thaliana

Abstract

Although cold acclimation is a key process in plants from temperate climates, the mechanisms sensing low temperature remain obscure. Here, we show that the accumulation of the organic acid fumaric acid, mediated by the cytosolic fumarase FUM2, is essential for cold acclimation of metabolism in the cold-tolerant model species Arabidopsis (Arabidopsis thaliana). A nontargeted metabolomic approach, using gas chromatography-mass spectrometry, identifies fumarate as a key component of the cold response in this species. Plants of T-DNA insertion mutants, lacking FUM2, show marked differences in their response to cold, with contrasting responses both in terms of metabolite concentrations and gene expression. The fum2 plants accumulated higher concentrations of phosphorylated sugar intermediates and of starch and malate. Transcripts for proteins involved in photosynthesis were markedly down-regulated in fum2.2 but not in wild-type Columbia-0. Plants of fum2 show a complete loss of the ability to acclimate photosynthesis to low temperature. We conclude that fumarate accumulation plays an essential role in low temperature sensing in Arabidopsis, either indirectly modulating metabolic or redox signals or possibly being itself directly involved in cold sensing.

The Role of Abscisic Acid Signaling in Maintaining the Metabolic Balance Required for Arabidopsis Growth under Nonstress Conditions

“…Because FUM2 is less highly induced by exogenous ABA in srk2d srk2e srk2i and areb than in wild type (Supplemental Figure 12), FUM2 expression in response to ABA might be regulated by the SnRK2-AREB/ABF signaling pathway. Intriguingly, FUM2 was recently shown to be essential for acclimation to low temperature, as the fum2 mutant is unable to modify its photosynthetic rate in response to the cold (Dyson et al, 2016). This is interesting in light of this study because of the similarities in the regulation of the responses to cold and osmotic stress and the finding that ABA is involved in both processes .…”

The complex allosteric and redox regulation of the fumarate hydratase and malate dehydratase reactions of Arabidopsis thaliana Fumarase 1 and 2 gives clues for understanding the massive accumulation of fumarate

“…Recently, Dyson et al . have provided compelling evidence that AtFUM2 is essential for A. thaliana acclimation to low temperatures. Moreover, biomass production at low temperatures exhibits a surprisingly high positive correlation with AtFUM2 transcript and fumarate levels .…”

“…Despite the fact that gene duplication has constituted the raw material for the adaptive evolution of new species, the processes by which duplicated genes become fixed in the genome were based on their ability to acquire either subfunctionalization or neofunctionalization [46]. Recently, Dyson et al [47] have provided compelling evidence that AtFUM2 is essential for A. thaliana acclimation to low temperatures. Moreover, biomass production at low temperatures exhibits a surprisingly high positive correlation with AtFUM2 transcript and fumarate levels [48].…”

Vacuolar invertase activity shapes photosynthetic stress response ofArabidopsis thalianaand stabilizes central energy supply

“…An explanation for these differences might be the recently described and naturally occurring promotor polymorphism of the Arabidopsis FUM2 gene (Riewe et al, 2016). The cytosolic fumarase, FUM2, catalyses the cytosolic interconversion of malate to fumarate and was shown to be essential for cold acclimation in Arabidopsis (Dyson et al, 2016). Riewe and colleagues found that the insertion/deletion polymorphism was absent from the promotor region of Columbia-0 FUM2, yet present in the C24 promotor region.…”