Rapid transcriptional and metabolic regulation of the deacclimation process in cold acclimated Arabidopsis thaliana

Abstract

BackgroundDuring low temperature exposure, temperate plant species increase their freezing tolerance in a process termed cold acclimation. This is accompanied by dampened oscillations of circadian clock genes and disrupted oscillations of output genes and metabolites. During deacclimation in response to warm temperatures, cold acclimated plants lose freezing tolerance and resume growth and development. While considerable effort has been directed toward understanding the molecular and metabolic basis of cold acclimation, much less information is available about the regulation of deacclimation.ResultsWe report metabolic (gas chromatography-mass spectrometry) and transcriptional (microarrays, quantitative RT-PCR) responses underlying deacclimation during the first 24 h after a shift of Arabidopsis thaliana (Columbia-0) plants cold acclimated at 4 °C back to warm temperature (20 °C). The data reveal a faster response of the transcriptome than of the metabolome and provide evidence for tightly regulated temporal responses at both levels. Metabolically, deacclimation is associated with decreasing contents of sugars, amino acids, glycolytic and TCA cycle intermediates, indicating an increased need for carbon sources and respiratory energy production for the activation of growth. The early phase of deacclimation also involves extensive down-regulation of protein synthesis and changes in the metabolism of lipids and cell wall components. Hormonal regulation appears particularly important during deacclimation, with extensive changes in the expression of genes related to auxin, gibberellin, brassinosteroid, jasmonate and ethylene metabolism. Members of several transcription factor families that control fundamental aspects of morphogenesis and development are significantly regulated during deacclimation, emphasizing that loss of freezing tolerance and growth resumption are transcriptionally highly interrelated processes. Expression patterns of some clock oscillator components resembled those under warm conditions, indicating at least partial re-activation of the circadian clock during deacclimation.ConclusionsThis study provides the first combined metabolomic and transcriptomic analysis of the regulation of deacclimation in cold acclimated plants. The data indicate cascades of rapidly regulated genes and metabolites that underlie the developmental switch resulting in reduced freezing tolerance and the resumption of growth. They constitute a large-scale dataset of genes, metabolites and pathways that are crucial during the initial phase of deacclimation. The data will be an important reference for further analyses of this and other important but under-researched stress deacclimation processes.Electronic supplementary materialThe online version of this article (10.1186/s12864-017-4126-3) contains supplementary material, which is available to authorized users.

Transcriptional and post-transcriptional regulation and transcriptional memory of chromatin regulators in response to low temperature

“…After 24 h of deacclimation, expression of the 440 investigated genes had largely returned to the NA status. This is in agreement to our earlier 441 data on the expression of genes encoding transcription factors, investigated by RT-qPCR, and 442 global gene expression, investigated by microarray hybridization(Pagter et al, 2017).…”

“…The quality of the cDNA was tested using primers amplifying the 3' and 5' region of GAPDH 202 (AT1G13440) (Zuther et al, 2012). cDNA of three independent biological replicates for each 203 time point was used for expression analysis (Pagter et al, 2017). 204…”

Arabidopsis REI-LIKE proteins activate ribosome biogenesis during cold acclimation

“…Cold acclimation of Arabidopsis has a well characterized carbohydrate component, where acclimating plants accumulate, e.g. (Kaplan et al, 2004; Kaplan et al, 2007) and deacclimating plants rapidly reduce endogenous sugar levels (Pagter et al, 2017). Adaptations in photosynthetic carbon metabolism provide signals that are integral part of Arabidopsis cold acclimation, including post transcriptional and transcriptional changes to sucrose metabolism (Stitt and Hurry, 2002).…”

Phytochrome light receptors control metabolic flux, and their action during seedling development sets the trajectory for biomass production

“…The metabolic profile of phy mutants is reminiscent of metabolic changes observed in response to drought, cold stress and ABA treatment (Cook et al 2004;Urano et al 2009;Kempa et al 2008;Pagter et al 2017). In particular, the two metabolites with the highest over-accumulation and synthetic rate, raffinose and proline, have been described as typical stress-induced metabolites in response to cold treatment or drought in Arabidopsis and other plants e.g.…”

“…Proline and raffinose accumulation typically occurs in abiotic stress conditions, such as cold stress, high salinity and drought (Kaplan et al 2004;Urano et al 2009;Kempa et al 2008;Pagter et al 2017). Synthesis of glutamine from glutamate is key for nitrogen assimilation into organic molecules and high nitrogen assimilation rates are predicted to occur during cold stress (Hildebrandt 2018).…”