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First published online February 22, 2005; 10.1104/pp.104.058354

Plant Physiology 137:961-968 (2005)
© 2005 American Society of Plant Biologists

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ENVIRONMENTAL STRESS AND ADAPTATION

Low Temperature Induction of Arabidopsis CBF1, 2, and 3 Is Gated by the Circadian Clock1

Sarah G. Fowler2, Daniel Cook2,3 and Michael F. Thomashow*

Michigan State University–U.S. Department of Energy Plant Research Laboratory (S.G.F., D.C., M.F.T.), and Department of Crop and Soil Sciences (M.F.T.), Michigan State University, East Lansing, Michigan 48824

Exposing Arabidopsis (Arabidopsis thaliana) plants to low temperature results in rapid induction of CBF1, 2, and 3 (CBF1-3; also known as DREB1B, C, and A, respectively), which encode transcriptional activators that induce expression of a battery of genes that increase plant freezing and chilling tolerance. Recently, it has been shown that basal levels of CBF3 transcripts and those of certain CBF-regulated genes exhibit circadian cycling. Here, we further explored the regulation of CBF1-3 by the circadian clock. The results indicated that the extent to which CBF1-3 transcripts accumulated in response to low temperature was dependent on the time of day that the plants were exposed to low temperature and that this was regulated by the circadian clock. The highest and lowest levels of cold-induced CBF1-3 transcript accumulation occurred at 4 and 16 h after subjective dawn, respectively. An analysis of CBF2 promoter-reporter gene fusions indicated that this control included transcriptional regulation. In addition, the cold responsiveness of RAV1 and ZAT12, genes that are cold induced in parallel with CBF1-3, was also subject to circadian regulation. However, whereas the maximum level of cold-induced RAV1 transcript accumulation occurred at the same time of day as did CBF1-3 transcripts, that of ZAT12 was in reverse phase, i.e. the highest level of cold-induced ZAT12 transcript accumulation occurred 16 h after subjective dawn. These results indicate that cold-induced expression of CBF1-3, RAV1, and ZAT12 is gated by the circadian clock and suggest that this regulation likely occurs through at least two nonidentical (though potentially overlapping) signaling pathways.

1 This work was supported by grants from the National Science Foundation Plant Genome project (grant no. DBI 0110124), the U.S. Department of Energy (grant no. DEFG0291ER20021), and the Michigan Agricultural Experiment Station.

2 These authors contributed equally to the paper.

3 Present address: U.S. Department of Agriculture Agricultural Research Service, Natural Products Utilization Research Unit, University, MS 38677.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.058354.

* Corresponding author; e-mail thomash6{at}msu.edu; fax 517–353–9168.

Received December 14, 2004; returned for revision December 30, 2004; accepted December 30, 2004.


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