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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.

Show MeSH
Integration of gene expression and metabolite accumulation for OAS.For transcripts, relative expression (log2) from a pool of five biological replicates is indicated. Metabolite content (log2) corresponds to the normalized peak apex intensities from five biological replicates with bars indicating the largest standard deviation. SAT, serine O-acetyltransferase (SAT1: At1g55920; SAT3: At3g13110); oas, cysteine synthase; OAS, O-acetylserine.
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pone-0014101-g008: Integration of gene expression and metabolite accumulation for OAS.For transcripts, relative expression (log2) from a pool of five biological replicates is indicated. Metabolite content (log2) corresponds to the normalized peak apex intensities from five biological replicates with bars indicating the largest standard deviation. SAT, serine O-acetyltransferase (SAT1: At1g55920; SAT3: At3g13110); oas, cysteine synthase; OAS, O-acetylserine.

Mentions: OAS is a direct precursor of cysteine. At 20°C, OAS pool sizes exhibited diurnal and circadian oscillations, peaking during the dark period (Figure 8). During cold treatment, levels of OAS strongly increased within a few hours and diurnal oscillations were observed. OAS is synthesized from serine by O-acetyltransferase (SAT). In plants at 20°C, SAT1 and SAT3 showed diurnal and circadian oscillations in expression with different phases. Interestingly, the peak expression of SAT3 occurred at the same phase as the maximum OAS levels. During cold acclimation, SAT3 expression increased, and SAT1 accumulation changed its phase. No changes in cysteine levels were observed (Figure 8) and several genes coding for cysteine synthase showed decreasing levels during cold acclimation (At2g43750, At3g59760, At4g14880 and At5g28020) (Table S2).


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)

Integration of gene expression and metabolite accumulation for OAS.For transcripts, relative expression (log2) from a pool of five biological replicates is indicated. Metabolite content (log2) corresponds to the normalized peak apex intensities from five biological replicates with bars indicating the largest standard deviation. SAT, serine O-acetyltransferase (SAT1: At1g55920; SAT3: At3g13110); oas, cysteine synthase; OAS, O-acetylserine.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0014101-g008: Integration of gene expression and metabolite accumulation for OAS.For transcripts, relative expression (log2) from a pool of five biological replicates is indicated. Metabolite content (log2) corresponds to the normalized peak apex intensities from five biological replicates with bars indicating the largest standard deviation. SAT, serine O-acetyltransferase (SAT1: At1g55920; SAT3: At3g13110); oas, cysteine synthase; OAS, O-acetylserine.
Mentions: OAS is a direct precursor of cysteine. At 20°C, OAS pool sizes exhibited diurnal and circadian oscillations, peaking during the dark period (Figure 8). During cold treatment, levels of OAS strongly increased within a few hours and diurnal oscillations were observed. OAS is synthesized from serine by O-acetyltransferase (SAT). In plants at 20°C, SAT1 and SAT3 showed diurnal and circadian oscillations in expression with different phases. Interestingly, the peak expression of SAT3 occurred at the same phase as the maximum OAS levels. During cold acclimation, SAT3 expression increased, and SAT1 accumulation changed its phase. No changes in cysteine levels were observed (Figure 8) and several genes coding for cysteine synthase showed decreasing levels during cold acclimation (At2g43750, At3g59760, At4g14880 and At5g28020) (Table S2).

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