Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock.
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.
Fowler
Sarah G
SG
Michigan State University-U.S. Department of Energy Plant Research Laboratory , Michigan State University, East Lansing, Michigan 48824, USA.
Cook
Daniel
D
Thomashow
Michael F
MF
D017360:Arabidopsis / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000096:biosynthesis*; D002940:Circadian Rhythm; D003080:Cold Temperature; D004268:DNA-Binding Proteins / Q000096:biosynthesis*; D018506:Gene Expression Regulation, Plant; D015398:Signal Transduction; D015534:Trans-Activators / Q000096:biosynthesis*; D014157:Transcription Factors / Q000096:biosynthesis*
D029681:Arabidopsis Proteins; C104387:CBF1 protein, Arabidopsis; C118228:CBF2 protein, Arabidopsis; D004268:DNA-Binding Proteins; C114578:DREB1A protein, Arabidopsis; C117695:RAV1 protein, Arabidopsis; D015534:Trans-Activators; D014157:Transcription Factors
Philos Trans R Soc Lond B Biol Sci. 2002 Jul 29;357(1423):831-47
12171647
Plant Physiol. 2004 Jul;135(3):1710-7
15247382
Plant Cell. 1997 Mar;9(3):297-304
9090876
Proc Natl Acad Sci U S A. 2002 Aug 20;99(17):11507-12
12165572
Plant Physiol. 2003 Oct;133(2):910-8
14500791
Plant J. 1998 Nov;16(4):433-42
9881163
Nat Biotechnol. 1999 Mar;17(3):287-91
10096298
Science. 2000 Dec 15;290(5499):2110-3
11118138
Dev Cell. 2002 May;2(5):629-41
12015970
Plant Physiol. 1993 Jan;101(1):31-36
12231662
Trends Plant Sci. 2002 Jan;7(1):4-6
11804815
Cell. 1998 Jun 26;93(7):1219-29
9657154
Dev Cell. 2002 May;2(5):516-8
12015957
Plant J. 1994 Jun;5(6):799-813
8054987
Mol Gen Genet. 1991 Mar;225(3):468-73
2017141
Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:571-599
15012220
Plant Physiol. 1999 Feb;119(2):463-70
9952441
Biol Chem. 1998 Jun;379(6):633-46
9687012
Plant J. 2004 Jun;38(6):982-93
15165189
Cell. 1998 Jun 26;93(7):1207-17
9657153
Plant J. 2005 Jan;41(2):195-211
15634197
Development. 1998 Feb;125(3):485-94
9425143
Proc Natl Acad Sci U S A. 2004 Mar 16;101(11):3985-90
15004278
Plant Cell. 2002 Aug;14(8):1675-90
12172015
Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):1035-40
9023378
Plant Cell. 1997 Apr;9(4):491-507
9144958
Annu Rev Physiol. 2001;63:677-94
11181972
Prog Clin Biol Res. 1987;227A:59-65
3601978
Proc Natl Acad Sci U S A. 2002 May 28;99(11):7786-91
12032361
J Biol Chem. 2004 Mar 19;279(12):11736-43
14722088
Plant Cell. 1994 Feb;6(2):251-64
8148648
Nucleic Acids Res. 1999 Jan 15;27(2):470-8
9862967
Science. 1998 Apr 3;280(5360):104-6
9525853
Plant Physiol. 2001 Jan;125(1):89-93
11154304
Plant Physiol. 1992 Dec;100(4):1780-6
16653197
Proc Natl Acad Sci U S A. 2003 May 27;100(11):6878-83
12736379
Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15491-6
8986839
Plant Cell. 1998 Aug;10(8):1391-406
9707537
Gene. 1992 Oct 21;120(2):313-4
1398145
Plant Physiol. 2000 Dec;124(4):1854-65
11115899
Plant Mol Biol. 1994 Mar;24(5):701-13
8193295
Plant Physiol. 2003 Jun;132(2):732-8
12805602
Plant Physiol. 1994 Mar;104(3):1015-25
7513083