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.
Highlights
Cold negatively affects plant growth and development
Long-day conditions were used for consistency with previous studies of metabolic changes associated with cold acclimation [4,5,7,14] and previous work on interactions between cold and the circadian clock [1,23,24]
One striking effect of low temperature is the disruption of circadian clock function, indicated by dampened or disrupted cycles of many clock components and output genes, in Arabidopsis [1], and in a tree [23,24]
Summary
Cold negatively affects plant growth and development. Many temperate plants, including Arabidopsis thaliana, increase their freezing tolerance after exposure to low, but non-freezing temperatures, in a process termed cold acclimation. CBFs are rapidly induced in cold, coordinating the expression of the ‘‘CBF regulon’’ which has a large effect on freezing tolerance [8,9]. Several studies have characterized the massive metabolic changes induced by cold [4,5,7,11,12,13,14,15]. These studies showed extensive modifications supporting cellular changes, increased antioxidant production and the accumulation of compatible solutes such as raffinose and proline. Metabolic reconfiguration during cold is dependent on stress duration [14] and developmental stage [14,15]
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