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Co-expression networks of deacclimation-impaired mutants identified involvement of hypoxia and complex regulation of the cold stress release response

ABSTRACT: Plants adapt to cold, non-freezing temperatures through cold acclimation and subsequently lose the acquired freezing tolerance in warmer temperatures in a process called deacclimation. By measuring the freezing tolerance of mutant lines, this study identified that the loss of HRA1, LBD41, MBF1c and JUB1 slows the rate of deacclimation in the first four days in Arabidopsis thaliana. Comparative transcriptomic (RNA-Seq) and co-expression analysis of Col-0, mbf1c and jub1 during deacclimation identified an involvement of thermoswitches, cell wall remodeler and transporters in the regulation of the rate of deacclimation. In mbf1c and jub1 a unique increase in stress responsive genes and regulation of the jasmonic acid pathway was detected and linked to the mutants’ retention of freezing tolerance during deacclimation. Hypoxia was observed to be induced in early deacclimation evidenced by an increase in ADH enzyme activity and upregulated gene expression of hypoxia markers (qRT-PCR). This work suggests that the overserved hypoxia response creates hypoxic niches within the plants and supports growth and development during deacclimation.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE196111 | GEO | 2022/09/30

REPOSITORIES: GEO

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Project description:During low temperature exposure, temperate plant species increase their freezing tolerance in a process termed cold acclimation. 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. Here, we report metabolic (GC-MS) and transcriptional (microarrays, qRT-PCR) responses underlying deacclimation during the first 24 h after a shift of cold acclimated Arabidopsis thaliana (Columbia-0) plants to warm temperature. The data revealed a faster response of the transcriptome than of the metabolome and provided evidence for tightly regulated temporal responses at both levels. Metabolically deacclimation is associated with decreasing contents of sugars, amino acids and glycolytic and TCA cycle intermediates, indicating an increased need for carbon sources and respiratory energy production associated with growth resumption under warm temperature conditions. Deacclimation also involves extensive down-regulation of protein synthesis and changes in the metabolism of lipids and cell wall components. Altered hormonal regulation appears particularly important during deacclimation, with changes in the expression of genes related to auxin, gibberellin, brassinosteroid, jasmonate and ethylene metabolisms. Several transcription factor families controlling fundamental aspects of plant development are significantly regulated during deacclimation, emphasizing that loss of freezing tolerance and growth resumption are interrelated processes that are transcriptionally highly interrelated. Expression patterns of some clock oscillator components during deacclimation resembled those under warm conditions, indicating at least partial re-activation of the circadian clock. This study provide the first comprehensive analysis of the regulation of deacclimation in cold acclimated plants. The data indicate cascades of rapidly regulated genes and metabolites that underly the developmental switch resulting in reduced freezing tolerance and the resumption of growth. They constitute a reference dataset of genes, metabolites and pathways that are crucial during the first rapid phase of deacclimation and will be useful for the further analysis of this important but under-researched plant process. We used whole genome microarrays to monitor changes in gene expression in the Arabidopsis thaliana accession Columbia-0 during the first 24 h after a shift of cold acclimated plants to warm temperature.

Project description:Intertidal zone organisms can experience transient freezing temperatures during winter low tides, but their extreme cold tolerance mechanisms are not known. Petrolisthes cinctipes is a temperate mid-high intertidal zone crab species that can experience wintertime habitat temperatures below the freezing point of seawater. We examined how cold tolerance changed during the initial phase of thermal acclimation to cold and warm temperatures, as well as the persistence of cold tolerance during long-term thermal acclimation. Thermal acclimation for as little as 6 hours at 8˚C enhanced crab tolerance during a 1h exposure to -2°C relative to crabs acclimated to 18˚C. Potential mechanisms for this enhanced tolerance were elucidated using cDNA microarrays to probe for differences in gene expression in cardiac tissue of warm and cold acclimated crabs during the first day of thermal acclimation. No changes in gene expression were detected until 12h of thermal acclimation. Genes strongly upregulated in warm acclimated crabs represented immune response and extracellular / intercellular processes, suggesting that warm acclimated crabs had a generalized stress response and may have been remodelling tissues or altering intercellular processes. Genes strongly upregulated in cold acclimated crabs included many that are involved in glucose production suggesting that cold acclimation involves increasing intracellular glucose as a cryoprotectant. Structural cytoskeletal proteins were also strongly represented among the genes upregulated in only cold acclimated crabs. There were no consistent changes in composition or the level of unsaturation of membrane phospholipid fatty acids with cold acclimation, which suggests that neither short- nor long-term changes in cold tolerance are mediated by changes in membrane fatty acid composition. Overall, our study demonstrates that initial changes in cold tolerance are likely not regulated by transcriptomic responses, but that gene expression-related changes in homeostasis begin within 12 hours – the length of a tidal cycle. all array data and raw images archived at the Porcelain Crab Array Database (http://array.sfsu.edu)

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Co-expression networks of deacclimation-impaired mutants identified involvement of hypoxia and complex regulation of the cold stress release response

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