Comparative analysis of gene expression under cold acclimation, deacclimation and reacclimation in Arabidopsis

Abstract

Cold acclimated plants show an elevated tolerance against subsequent cold stress. Such adaptation requires alterations in gene expression as well as physiological changes. We were interested in gene expression changes at the transcriptional level during adaptation processes. The patterns of transcriptional changes associated with cold acclimation, deacclimation and reacclimation in Arabidopsis leaves were characterized using the Coldstresschip. Gene expression profiles were further analyzed by 'coexpressed gene sets' using gene set enrichment analysis (GSEA). Genes involved in signal transduction through calcium, and cascades of kinases and transcription factor genes, were distinctively induced in the early response of cold acclimation. On the other hand, genes involved in antioxidation, cell wall biogenesis and sterol synthesis were upregulated in the late response of cold acclimation. After the removal of cold, the expression patterns of most genes rapidly returned to the original states. However, photosynthetic light-harvesting complex genes and lipid metabolism-related genes stayed upregulated in cold deacclimated plants compared to non-treated plants. It is also notable that many well-known cold-inducible genes are slightly induced in reacclimation and their expression remains at relatively low levels in cold reacclimation compared to the expression during the first cold acclimation. The results in this study show the dynamic nature of gene expression occurring during cold acclimation, deacclimation and reacclimation. Our results suggest that there is a memory of cold stress and that the 'memory of cold stress' is possibly due to elevated photosynthetic efficiency, modified lipid metabolism, increased calcium signaling, pre-existing defense protein made during first cold acclimation and/or modified signal transduction from pre-existing defense protein.

Delayed response to cold stress is characterized by successive metabolic shifts culminating in apple fruit peel necrosis

“…Chlorophyll content was altered as the tissue became necrotic during symptom development. Reduced expression of genes involved in photosynthesis during exposure to cold temperatures has been reported in Arabidopsis [46], which becomes increasingly less dramatic with sequential acclimation events [47]. Altered photosynthetic gene expression may be linked with changes in saturation [48] or constituency of phytosterol membrane components [21] during apple ripening and storage that are important for membrane fluidity and function in other plant species and tissues [49, 50].…”

Acclimation, priming and memory in the response of Arabidopsis thaliana seedlings to cold stress

“…A variety of mechanisms have been shown to be involved in priming stress responses, ranging from lasting changes in metabolism to modification of transcriptions factors and chromatin changes 31,32 . Priming of the response to cold stress has been shown to be regulated by tAPX 29 and to be associated with partly accession-specific changes of transcripts and metabolites 14,33,34 . However, genes important for cold memory have as yet not been described while several genes are known that play a role in maintaining a primed state in response to elevated temperatures.…”

Transcriptional and Post-Transcriptional Regulation and Transcriptional Memory of Chromatin Regulators in Response to Low Temperature

“…Changes in the transcriptional activity of cold-stress-responsive genes upon exposure to low temperatures might be partly achieved through remodeling of the chromatin, rendering it more or less accessible for the transcriptional machinery, thereby affecting the expression levels of the genes. After cold stress ends and deacclimation begins, most stress-responsive genes return quickly back to their initial transcriptional levels (Byun et al, 2014;Pagter et al, 2017), suggesting that coldinduced changes to the chromatin might be reversed during deacclimation. Cold induced changes to the chromatin have in particular been studied in the context of vernalization.…”