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Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis.

Espinoza C, Degenkolbe T, Caldana C, Zuther E, Leisse A, Willmitzer L, Hincha DK, Hannah MA - PLoS ONE (2010)

Bottom Line: Levels of some conventional cold induced metabolites, such as γ-aminobutyric acid, galactinol, raffinose and putrescine, exhibited diurnal and circadian oscillations and transcripts encoding their biosynthetic enzymes often also cycled and preceded their cold-induction, in agreement with transcriptional regulation.However, the accumulation of other cold-responsive metabolites, for instance homoserine, methionine and maltose, did not have consistent transcriptional regulation, implying that metabolic reconfiguration involves complex transcriptional and post-transcriptional mechanisms.These data demonstrate the importance of understanding cold acclimation in the correct day-night context, and are further supported by our demonstration of impaired cold acclimation in a circadian mutant.

View Article: PubMed Central - PubMed

Affiliation: Max-Planck-Institute of Molecular Plant Physiology, Potsdam, Germany.

ABSTRACT
In plants, there is a large overlap between cold and circadian regulated genes and in Arabidopsis, we have shown that cold (4°C) affects the expression of clock oscillator genes. However, a broader insight into the significance of diurnal and/or circadian regulation of cold responses, particularly for metabolic pathways, and their physiological relevance is lacking. Here, we performed an integrated analysis of transcripts and primary metabolites using microarrays and gas chromatography-mass spectrometry. As expected, expression of diurnally regulated genes was massively affected during cold acclimation. Our data indicate that disruption of clock function at the transcriptional level extends to metabolic regulation. About 80% of metabolites that showed diurnal cycles maintained these during cold treatment. In particular, maltose content showed a massive night-specific increase in the cold. However, under free-running conditions, maltose was the only metabolite that maintained any oscillations in the cold. Furthermore, although starch accumulates during cold acclimation we show it is still degraded at night, indicating significance beyond the previously demonstrated role of maltose and starch breakdown in the initial phase of cold acclimation. Levels of some conventional cold induced metabolites, such as γ-aminobutyric acid, galactinol, raffinose and putrescine, exhibited diurnal and circadian oscillations and transcripts encoding their biosynthetic enzymes often also cycled and preceded their cold-induction, in agreement with transcriptional regulation. However, the accumulation of other cold-responsive metabolites, for instance homoserine, methionine and maltose, did not have consistent transcriptional regulation, implying that metabolic reconfiguration involves complex transcriptional and post-transcriptional mechanisms. These data demonstrate the importance of understanding cold acclimation in the correct day-night context, and are further supported by our demonstration of impaired cold acclimation in a circadian mutant.

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Core network of metabolite correlations observed in diurnal and circadian conditions both at 20°C and 4°C.In the depicted network, nodes (spots) represent metabolites and edges (lines) indicate highly significant positive (blue) and negative (red) pairwise correlations between metabolites. The core network represents thirteen correlations between seventeen metabolites which were stably in diurnal and circadian conditions both at 20°C and 4°C (i.e. in all four studied time series). Node color codes indicate compound classes as described in the figure. The significance threshold of the Spearman correlations was set at <0.001 for the Bonferroni corrected p-values (see Methods).
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pone-0014101-g005: Core network of metabolite correlations observed in diurnal and circadian conditions both at 20°C and 4°C.In the depicted network, nodes (spots) represent metabolites and edges (lines) indicate highly significant positive (blue) and negative (red) pairwise correlations between metabolites. The core network represents thirteen correlations between seventeen metabolites which were stably in diurnal and circadian conditions both at 20°C and 4°C (i.e. in all four studied time series). Node color codes indicate compound classes as described in the figure. The significance threshold of the Spearman correlations was set at <0.001 for the Bonferroni corrected p-values (see Methods).

Mentions: In addition, the core network, representing the metabolite-metabolite correlations that were stably present under all experimental conditions, revealed biologically relevant modules (Figure 5). Thirteen edges connecting 17 metabolites were present under all experimental conditions, such as glutamine – asparagine, raffinose – galactinol, phenylalanine – tyrosine, leucine – isoleucine, glucose – fructose and 4-hydroxycinnamic acid – 4-hydroxybenzoic acid. In the 20°C L/L network an amino acid-dominated module was present consisting of branched-chain (isoleucine, leucine and valine) and aromatic (phenylalanine and tyrosine) amino acids, beta-alanine and lysine. In L/D they were additionally connected to other amino acids as well as organic acids such as 2-oxoglutaric acid, pyruvic acid and glycolic acid. Maltose was positively correlated to amino acids in L/L, whereas it was negatively correlated in L/D. Under both light conditions the known stress responsive metabolites raffinose, putrescine, proline, galactinol, trehalose and GABA were more highly connected at 4°C than at 20°C, indicating coordinated stress responses of metabolism.


Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis.

Espinoza C, Degenkolbe T, Caldana C, Zuther E, Leisse A, Willmitzer L, Hincha DK, Hannah MA - PLoS ONE (2010)

Core network of metabolite correlations observed in diurnal and circadian conditions both at 20°C and 4°C.In the depicted network, nodes (spots) represent metabolites and edges (lines) indicate highly significant positive (blue) and negative (red) pairwise correlations between metabolites. The core network represents thirteen correlations between seventeen metabolites which were stably in diurnal and circadian conditions both at 20°C and 4°C (i.e. in all four studied time series). Node color codes indicate compound classes as described in the figure. The significance threshold of the Spearman correlations was set at <0.001 for the Bonferroni corrected p-values (see Methods).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2990718&req=5

pone-0014101-g005: Core network of metabolite correlations observed in diurnal and circadian conditions both at 20°C and 4°C.In the depicted network, nodes (spots) represent metabolites and edges (lines) indicate highly significant positive (blue) and negative (red) pairwise correlations between metabolites. The core network represents thirteen correlations between seventeen metabolites which were stably in diurnal and circadian conditions both at 20°C and 4°C (i.e. in all four studied time series). Node color codes indicate compound classes as described in the figure. The significance threshold of the Spearman correlations was set at <0.001 for the Bonferroni corrected p-values (see Methods).
Mentions: In addition, the core network, representing the metabolite-metabolite correlations that were stably present under all experimental conditions, revealed biologically relevant modules (Figure 5). Thirteen edges connecting 17 metabolites were present under all experimental conditions, such as glutamine – asparagine, raffinose – galactinol, phenylalanine – tyrosine, leucine – isoleucine, glucose – fructose and 4-hydroxycinnamic acid – 4-hydroxybenzoic acid. In the 20°C L/L network an amino acid-dominated module was present consisting of branched-chain (isoleucine, leucine and valine) and aromatic (phenylalanine and tyrosine) amino acids, beta-alanine and lysine. In L/D they were additionally connected to other amino acids as well as organic acids such as 2-oxoglutaric acid, pyruvic acid and glycolic acid. Maltose was positively correlated to amino acids in L/L, whereas it was negatively correlated in L/D. Under both light conditions the known stress responsive metabolites raffinose, putrescine, proline, galactinol, trehalose and GABA were more highly connected at 4°C than at 20°C, indicating coordinated stress responses of metabolism.

Bottom Line: Levels of some conventional cold induced metabolites, such as γ-aminobutyric acid, galactinol, raffinose and putrescine, exhibited diurnal and circadian oscillations and transcripts encoding their biosynthetic enzymes often also cycled and preceded their cold-induction, in agreement with transcriptional regulation.However, the accumulation of other cold-responsive metabolites, for instance homoserine, methionine and maltose, did not have consistent transcriptional regulation, implying that metabolic reconfiguration involves complex transcriptional and post-transcriptional mechanisms.These data demonstrate the importance of understanding cold acclimation in the correct day-night context, and are further supported by our demonstration of impaired cold acclimation in a circadian mutant.

View Article: PubMed Central - PubMed

Affiliation: Max-Planck-Institute of Molecular Plant Physiology, Potsdam, Germany.

ABSTRACT
In plants, there is a large overlap between cold and circadian regulated genes and in Arabidopsis, we have shown that cold (4°C) affects the expression of clock oscillator genes. However, a broader insight into the significance of diurnal and/or circadian regulation of cold responses, particularly for metabolic pathways, and their physiological relevance is lacking. Here, we performed an integrated analysis of transcripts and primary metabolites using microarrays and gas chromatography-mass spectrometry. As expected, expression of diurnally regulated genes was massively affected during cold acclimation. Our data indicate that disruption of clock function at the transcriptional level extends to metabolic regulation. About 80% of metabolites that showed diurnal cycles maintained these during cold treatment. In particular, maltose content showed a massive night-specific increase in the cold. However, under free-running conditions, maltose was the only metabolite that maintained any oscillations in the cold. Furthermore, although starch accumulates during cold acclimation we show it is still degraded at night, indicating significance beyond the previously demonstrated role of maltose and starch breakdown in the initial phase of cold acclimation. Levels of some conventional cold induced metabolites, such as γ-aminobutyric acid, galactinol, raffinose and putrescine, exhibited diurnal and circadian oscillations and transcripts encoding their biosynthetic enzymes often also cycled and preceded their cold-induction, in agreement with transcriptional regulation. However, the accumulation of other cold-responsive metabolites, for instance homoserine, methionine and maltose, did not have consistent transcriptional regulation, implying that metabolic reconfiguration involves complex transcriptional and post-transcriptional mechanisms. These data demonstrate the importance of understanding cold acclimation in the correct day-night context, and are further supported by our demonstration of impaired cold acclimation in a circadian mutant.

Show MeSH
Related in: MedlinePlus