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PMID: 21124901 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

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

PloS one ·Vol. 5 ·No. 11 ·2010-11-23 ·Pages e14101

Espinoza C, Degenkolbe T, Caldana C, Zuther E, Leisse A, Willmitzer L, Hincha DK, Hannah MA

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.

MeSH Terms
Acclimatization Arabidopsis/genetics,growth & development,metabolism Arabidopsis Proteins/genetics,metabolism Circadian Rhythm Cold Temperature Darkness Gene Expression Profiling Gene Expression Regulation, Developmental/radiation effects Gene Expression Regulation, Plant/radiation effects Light Metabolomics/methods Mutation Photoperiod
Chemicals
Arabidopsis Proteins
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Espinoza Carmen
Max-Planck-Institute of Molecular Plant Physiology, Potsdam, Germany.
Degenkolbe Thomas
Caldana Camila
Zuther Ellen
Leisse Andrea
Willmitzer Lothar
Hincha Dirk K
Hannah Matthew A
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Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
DOI
10.1371/journal.pone.0014101
Published
2010-11-23
Epub
2010-00-23
Pages
e14101
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC2990718
Subset
IM
External Links
PubMed source DOI: 10.1371/journal.pone.0014101 PMC Full Text View journal details
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