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

MPS-Authors
http://pubman.mpdl.mpg.de/cone/persons/resource/persons129748

Espinoza,  C.
Transcript Profiling, Infrastructure Groups and Service Units, Max Planck Institute of Molecular Plant Physiology, Max Planck Society;

http://pubman.mpdl.mpg.de/cone/persons/resource/persons97118

Degenkolbe,  T.
Transcript Profiling, Infrastructure Groups and Service Units, Max Planck Institute of Molecular Plant Physiology, Max Planck Society;

http://pubman.mpdl.mpg.de/cone/persons/resource/persons97097

Caldana,  C.
Small Molecules, Department Willmitzer, Max Planck Institute of Molecular Plant Physiology, Max Planck Society;

http://pubman.mpdl.mpg.de/cone/persons/resource/persons97500

Zuther,  E.
Transcript Profiling, Infrastructure Groups and Service Units, Max Planck Institute of Molecular Plant Physiology, Max Planck Society;

http://pubman.mpdl.mpg.de/cone/persons/resource/persons97270

Leisse,  A.
Small Molecules, Department Willmitzer, Max Planck Institute of Molecular Plant Physiology, Max Planck Society;

http://pubman.mpdl.mpg.de/cone/persons/resource/persons97481

Willmitzer,  L.
Small Molecules, Department Willmitzer, Max Planck Institute of Molecular Plant Physiology, Max Planck Society;

http://pubman.mpdl.mpg.de/cone/persons/resource/persons97195

Hincha,  D. K.
Transcript Profiling, Infrastructure Groups and Service Units, Max Planck Institute of Molecular Plant Physiology, Max Planck Society;

http://pubman.mpdl.mpg.de/cone/persons/resource/persons97182

Hannah,  M. A.
Small Molecules, Department Willmitzer, Max Planck Institute of Molecular Plant Physiology, Max Planck Society;

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Citation

Espinoza, C., Degenkolbe, T., Caldana, C., Zuther, E., Leisse, A., Willmitzer, L., et al. (2010). Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. PLoS One, 5(11), e14101. doi:10.1371/journal.pone.0014101.


Cite as: http://hdl.handle.net/11858/00-001M-0000-0014-241D-2
Abstract
In plants, there is a large overlap between cold and circadian regulated genes and in Arabidopsis, we have shown that cold (4 degrees 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 gamma-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.