Transcriptomic and Metabolomic Approaches to the Analysis of Plant Freezing Tolerance and Cold Acclimation

Hincha, Dirk K.; Espinoza, Carmen; Zuther, Ellen

doi:10.1002/9783527632930.ch11

Cited by 29 publications

(20 citation statements)

References 189 publications

(258 reference statements)

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“…Transcriptomic, lipidomic, and metabolomic changes during cold exposure of Arabidopsis plants have been described in detail before (see Chinnusamy et al, ; Guy, Kaplan, Kopka, Selbig, & Hincha, ; Hincha et al, ; Thomashow, , for reviews). We will therefore not discuss general cold responses but rather focus on aspects that are directly related to cold memory.…”

Section: Discussionmentioning

confidence: 99%

“…The process of cold acclimation has been extensively investigated, in particular in Arabidopsis thaliana (for reviews, see Chinnusamy, Zhu, & Zhu, , Gilmour, Fowler, & Thomashow, ). It involves a multitude of adaptations including induction of C‐repeat binding factor transcription factors and their downstream genes, lipid remodelling, accumulation of compatible solutes, and cold‐regulated proteins (Hincha, Espinoza, & Zuther, ; Xin & Browse, ). On the other hand, the molecular mechanisms underlying the regulation of the loss of freezing tolerance during the lag or memory phase are only poorly understood, despite their ecological and agronomic importance (Zuther, Juszczak, Lee, Baier, & Hincha, ).…”

Section: Introductionmentioning

confidence: 99%

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Molecular signatures associated with increased freezing tolerance due to low temperature memory in Arabidopsis

Zuther

Schaarschmidt

Fischer

et al. 2019

Plant Cell & Environment

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Alternating temperatures require fast and coordinated adaptation responses of plants.Cold acclimation has been extensively investigated and results in increased freezing tolerance in Arabidopsis thaliana. Here, we show that the two Arabidopsis accessions, Col-0 and N14, which differ in their freezing tolerance, showed memory of cold acclimation, that is, cold priming. Freezing tolerance was higher in plants exposed to cold priming at 4°C, a lag phase at 20°C, and a second triggering cold stress (4°C) than in plants that were only cold primed. To our knowledge, this is the first report on cold memory improving plant freezing tolerance. The triggering response was distinguishable from the priming response at the levels of gene expression (RNA-Seq), lipid (ultraperformance liquid chromatography-mass spectrometry), and metabolite composition (gas chromatography-mass spectrometry). Transcriptomic responses pointed to induced lipid, secondary metabolism, and stress in Col-0 and growth-related functions in N14. Specific accumulation of lipids included arabidopsides with possible functions as signalling molecules or precursors of jasmonic acid. Whereas cold-induced metabolites such as raffinose and its precursors were maintained in N14 during the lag phase, they were strongly accumulated in Col-0 after the cold trigger. This indicates genetic differences in the transcriptomic and metabolic patterns during cold memory.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Molecular signatures associated with increased freezing tolerance due to low temperature memory in Arabidopsis

Zuther

Schaarschmidt

Fischer

et al. 2019

Plant Cell & Environment

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“…For instance, several works suggested that cold triggers a highly complex regulatory program that results in extensive reorganization of the transcriptome (Oono et al, 2006; Chinnusamy et al, 2007; Hincha et al, 2012). These changes involve up- and down-regualtion of hundreds of genes occurring in waves with time of incubating plants at low temperature.…”

Section: Introductionmentioning

confidence: 99%

“…Despite CA complexity mentioned above, recent technical advances in genetic analysis tools, gene expression profiling, and metabolomics have made it possible to dissect the complex processes involved in plant CA (Jozefczuk et al, 2010; Hincha et al, 2012; Sinha et al, 2015). Transcriptome- and metabolome-wide approaches can allow visualization of the underlying biological processes of cold stress, leading to a better insight into the behavior responses to CA.…”

Section: Introductionmentioning

confidence: 99%

Insights from the Cold Transcriptome and Metabolome of Dendrobium officinale: Global Reprogramming of Metabolic and Gene Regulation Networks during Cold Acclimation

Chen

et al. 2016

Front. Plant Sci.

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Plant cold acclimation (CA) is a genetically complex phenomenon involving gene regulation and expression. Little is known about the cascading pattern of gene regulatroy network and the link between genes and metabolites during CA. Dendrobium officinale (DOKM) is an important medicinal and ornamental plant and hypersensitive to low temperature. Here, we used the large scale metabolomic and transcriptomic technologies to reveal the response to CA in DOKM seedlings based on the physiological profile analyses. Lowering temperature from 4 to –2°C resulted in significant increase (P < 0.01) in antioxidant activities and electrolyte leakage (EL) during 24 h. The fitness CA piont of 0°C and control (20°C) during 20 h were firstly obtained according to physiological analyses. Subsequently, massive transcriptome and metabolome reprogramming occurred during CA. The gene to metabolite network demonstrated that the CA associated processes are highly energy demanding through activating hydrolysis of sugars, amino acids catabolism and citrate cycle. The expression levels of 2,767 genes were significantly affected by CA, including 153-fold upregulation of CBF transcription factor, 56-fold upregulation of MAPKKK16 protein kinase. Moreover, the gene interaction and regulation network analysis revealed that the CA as an active process, was regulated at the transcriptional, post-transcriptional, translational and post-translational levels. Our findings highligted a comprehensive regulatory mechanism including cold signal transduction, transcriptional regulation, and gene expression, which contributes a deeper understanding of the highly complex regulatory program during CA in DOKM. Some marker genes identified in DOKM seedlings will allow us to understand the role of each individual during CA by further functional analyses.

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“…Plants native to temperate and boreal climates are challenged with seasonal low temperatures that may result in freezing stress, i.e., the crystallization of ice in the intercellular spaces, in particular in the exposed above-ground tissues. Such plant species are able to increase their freezing tolerance in fall in response to low temperatures above the freezing point in a process termed cold acclimation (1)(2)(3). In the model plant Arabidopsis thaliana, massive changes in gene expression occur during cold acclimation, leading, among other reactions, to the accumulation of cold-regu-lated (COR) proteins (4).…”

Section: Introductionmentioning

confidence: 99%

Folding and Lipid Composition Determine Membrane Interaction of the Disordered Protein COR15A

Navarro‐Retamal

Bremer

Ingólfsson

et al. 2018

Biophysical Journal

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Plants from temperate climates, such as the model plant Arabidopsis thaliana, are challenged with seasonal low temperatures that lead to increased freezing tolerance in fall in a process termed cold acclimation. Among other adaptations, this involves the accumulation of cold-regulated (COR) proteins, such as the intrinsically disordered chloroplast-localized protein COR15A. Together with its close homolog COR15B, it stabilizes chloroplast membranes during freezing. COR15A folds into amphipathic α-helices in the presence of high concentrations of low-molecular-mass crowders or upon dehydration. Under these conditions, the (partially) folded protein binds peripherally to membranes. In our study, we have used coarse-grained molecular dynamics simulations to elucidate the details of COR15A-membrane binding and its effects on membrane structure and dynamics. Simulation results indicate that at least partial folding of COR15A and the presence of highly unsaturated galactolipids in the membranes are necessary for efficient membrane binding. The bound protein is stabilized on the membrane by interactions of charged and polar amino acids with galactolipid headgroups and by interactions of hydrophobic amino acids with the upper part of the fatty acyl chains. Experimentally, the presence of liposomes made from a mixture of lipids mimicking chloroplast membranes induces additional folding in COR15A under conditions of partial dehydration, in agreement with the simulation results.

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Transcriptomic and Metabolomic Approaches to the Analysis of Plant Freezing Tolerance and Cold Acclimation

Cited by 29 publications

References 189 publications

Molecular signatures associated with increased freezing tolerance due to low temperature memory in Arabidopsis

Molecular signatures associated with increased freezing tolerance due to low temperature memory in Arabidopsis

Insights from the Cold Transcriptome and Metabolome of Dendrobium officinale: Global Reprogramming of Metabolic and Gene Regulation Networks during Cold Acclimation

Folding and Lipid Composition Determine Membrane Interaction of the Disordered Protein COR15A

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