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First published online July 25, 2002; 10.1105/tpc.003483

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The Plant Cell, Vol. 14, 1675-1690, August 2002, Copyright © 2002,
American Society of Plant Biologists


GENOMICS ARTICLE

Arabidopsis Transcriptome Profiling Indicates That Multiple Regulatory Pathways Are Activated during Cold Acclimation in Addition to the CBF Cold Response Pathway

Sarah Fowler and Michael F. Thomashow1

Michigan State University–Department of Energy Plant Research Laboratory and Department of Crop and Soil Sciences, Michigan State University, East Lansing, Michigan 48824-1312

1 To whom correspondence should be addressed. E-mail thomash6{at}msu.edu; fax 517-353-9168

Many plants, including Arabidopsis, increase in freezing tolerance in response to low, nonfreezing temperatures, a phenomenon known as cold acclimation. Previous studies established that cold acclimation involves rapid expression of the CBF transcriptional activators (also known as DREB1 proteins) in response to low temperature followed by induction of the CBF regulon (CBF-targeted genes), which contributes to an increase in freezing tolerance. Here, we present the results of transcriptome-profiling experiments indicating the existence of multiple low-temperature regulatory pathways in addition to the CBF cold response pathway. The transcript levels of ~8000 genes were determined at multiple times after plants were transferred from warm to cold temperature and in warm-grown plants that constitutively expressed CBF1, CBF2, or CBF3. A total of 306 genes were identified as being cold responsive, with transcripts for 218 genes increasing and those for 88 genes decreasing threefold or more at one or more time points during the 7-day experiment. These results indicate that extensive downregulation of gene expression occurs during cold acclimation. Of the cold-responsive genes, 48 encode known or putative transcription factors. Two of these, RAP2.1 and RAP2.6, were activated by CBF expression and thus presumably control subregulons of the CBF regulon. Transcriptome comparisons indicated that only 12% of the cold-responsive genes are certain members of the CBF regulon. Moreover, at least 28% of the cold-responsive genes were not regulated by the CBF transcription factors, including 15 encoding known or putative transcription factors, indicating that these cold-responsive genes are members of different low-temperature regulons. Significantly, CBF expression at warm temperatures repressed the expression of eight genes that also were downregulated by low temperature, indicating that in addition to gene induction, gene repression is likely to play an integral role in cold acclimation.




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Plant Physiol.Home page
F. Kaplan, J. Kopka, D. W. Haskell, W. Zhao, K. C. Schiller, N. Gatzke, D. Y. Sung, and C. L. Guy
Exploring the Temperature-Stress Metabolome of Arabidopsis
Plant Physiology, December 1, 2004; 136(4): 4159 - 4168.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
T. Puhakainen, C. Li, M. Boije-Malm, J. Kangasjarvi, P. Heino, and E. T. Palva
Short-Day Potentiation of Low Temperature-Induced Gene Expression of a C-Repeat-Binding Factor-Controlled Gene during Cold Acclimation in Silver Birch
Plant Physiology, December 1, 2004; 136(4): 4299 - 4307.
[Abstract] [Full Text] [PDF]


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J Exp BotHome page
E. A. Bray
Genes commonly regulated by water-deficit stress in Arabidopsis thaliana
J. Exp. Bot., November 1, 2004; 55(407): 2331 - 2341.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
J. Browse and B. M. Lange
Counting the cost of a cold-blooded life: Metabolomics of cold acclimation
PNAS, October 19, 2004; 101(42): 14996 - 14997.
[Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
D. Cook, S. Fowler, O. Fiehn, and M. F. Thomashow
From The Cover: A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis
PNAS, October 19, 2004; 101(42): 15243 - 15248.
[Abstract] [Full Text] [PDF]


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Plant CellHome page
L.-S. P. Tran, K. Nakashima, Y. Sakuma, S. D. Simpson, Y. Fujita, K. Maruyama, M. Fujita, M. Seki, K. Shinozaki, and K. Yamaguchi-Shinozaki
Isolation and Functional Analysis of Arabidopsis Stress-Inducible NAC Transcription Factors That Bind to a Drought-Responsive cis-Element in the early responsive to dehydration stress 1 Promoter
PLANT CELL, September 1, 2004; 16(9): 2481 - 2498.
[Abstract] [Full Text] [PDF]


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Plant Cell PhysiolHome page
F. Qin, Y. Sakuma, J. Li, Q. Liu, Y.-Q. Li, K. Shinozaki, and K. Yamaguchi-Shinozaki
Cloning and Functional Analysis of a Novel DREB1/CBF Transcription Factor Involved in Cold-Responsive Gene Expression in Zea mays L.
Plant Cell Physiol., August 15, 2004; 45(8): 1042 - 1052.
[Abstract] [Full Text] [PDF]


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Plant CellHome page
G. Thorlby, N. Fourrier, and G. Warren
The SENSITIVE TO FREEZING2 Gene, Required for Freezing Tolerance in Arabidopsis thaliana, Encodes a {beta}-Glucosidase
PLANT CELL, August 1, 2004; 16(8): 2192 - 2203.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
P. Boominathan, R. Shukla, A. Kumar, D. Manna, D. Negi, P. K. Verma, and D. Chattopadhyay
Long Term Transcript Accumulation during the Development of Dehydration Adaptation in Cicer arietinum
Plant Physiology, July 1, 2004; 135(3): 1608 - 1620.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
F. Kaplan and C. L. Guy
{beta}-Amylase Induction and the Protective Role of Maltose during Temperature Shock
Plant Physiology, July 1, 2004; 135(3): 1674 - 1684.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
J. Zhu, H. Shi, B.-h. Lee, B. Damsz, S. Cheng, V. Stirm, J.-K. Zhu, P. M. Hasegawa, and R. A. Bressan
An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway
PNAS, June 29, 2004; 101(26): 9873 - 9878.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
J. Z. Zhang, R. A. Creelman, and J.-K. Zhu
From Laboratory to Field. Using Information from Arabidopsis to Engineer Salt, Cold, and Drought Tolerance in Crops
Plant Physiology, June 1, 2004; 135(2): 615 - 621.
[Full Text] [PDF]


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J. Biol. Chem.Home page
L. Rizhsky, S. Davletova, H. Liang, and R. Mittler
The Zinc Finger Protein Zat12 Is Required for Cytosolic Ascorbate Peroxidase 1 Expression during Oxidative Stress in Arabidopsis
J. Biol. Chem., March 19, 2004; 279(12): 11736 - 11743.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
F. Novillo, J. M. Alonso, J. R. Ecker, and J. Salinas
CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis
PNAS, March 16, 2004; 101(11): 3985 - 3990.
[Abstract] [Full Text] [PDF]


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Plant Cell PhysiolHome page
M. Kasuga, S. Miura, K. Shinozaki, and K. Yamaguchi-Shinozaki
A Combination of the Arabidopsis DREB1A Gene and Stress-Inducible rd29A Promoter Improved Drought- and Low-Temperature Stress Tolerance in Tobacco by Gene Transfer
Plant Cell Physiol., March 15, 2004; 45(3): 346 - 350.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
H. Shou, P. Bordallo, J.-B. Fan, J. M. Yeakley, M. Bibikova, J. Sheen, and K. Wang
From The Cover: Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize
PNAS, March 2, 2004; 101(9): 3298 - 3303.
[Abstract] [Full Text] [PDF]


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J Exp BotHome page
A. Welling, P. Rinne, A. Vihera-Aarnio, S. Kontunen-Soppela, P. Heino, and E. T. Palva
Photoperiod and temperature differentially regulate the expression of two dehydrin genes during overwintering of birch (Betula pubescens Ehrh.)
J. Exp. Bot., February 1, 2004; 55(396): 507 - 516.
[Abstract] [Full Text] [PDF]


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Plant CellHome page
Y. Yamauchi, M. Ogawa, A. Kuwahara, A. Hanada, Y. Kamiya, and S. Yamaguchi
Activation of Gibberellin Biosynthesis and Response Pathways by Low Temperature during Imbibition of Arabidopsis thaliana Seeds
PLANT CELL, February 1, 2004; 16(2): 367 - 378.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
J. I. Watkinson, A. A. Sioson, C. Vasquez-Robinet, M. Shukla, D. Kumar, M. Ellis, L. S. Heath, N. Ramakrishnan, B. Chevone, L. T. Watson, et al.
Photosynthetic Acclimation Is Reflected in Specific Patterns of Gene Expression in Drought-Stressed Loblolly Pine
Plant Physiology, December 1, 2003; 133(4): 1702 - 1716.
[Abstract] [Full Text]


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Plant Physiol.Home page
J. C. Pennycooke, M. L. Jones, and C. Stushnoff
Down-Regulating {alpha}-Galactosidase Enhances Freezing Tolerance in Transgenic Petunia
Plant Physiology, October 1, 2003; 133(2): 901 - 909.
[Abstract] [Full Text] [PDF]


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Plant Cell PhysiolHome page
T. Takagi, M. Nakamura, H. Hayashi, R. Inatsugi, R. Yano, and I. Nishida
The Leaf-Order-Dependent Enhancement of Freezing Tolerance in Cold-Acclimated Arabidopsis Rosettes is not Correlated with the Transcript Levels of the Cold-Inducible Transcription Factors of CBF/DREB1
Plant Cell Physiol., September 15, 2003; 44(9): 922 - 931.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
F. T.S. Nogueira, V. E. De Rosa Jr., M. Menossi, E. C. Ulian, and P. Arruda
RNA Expression Profiles and Data Mining of Sugarcane Response to Low Temperature
Plant Physiology, August 1, 2003; 132(4): 1811 - 1824.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
M. Suzuki, M. G. Ketterling, Q.-B. Li, and D. R. McCarty
Viviparous1 Alters Global Gene Expression Patterns through Regulation of Abscisic Acid Signaling
Plant Physiology, July 1, 2003; 132(3): 1664 - 1677.
[Abstract] [Full Text] [PDF]


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J Exp BotHome page
S. R. Tabaei-Aghdaei, R. S. Pearce, and P. Harrison
Sugars regulate cold-induced gene expression and freezing-tolerance in barley cell cultures
J. Exp. Bot., June 1, 2003; 54(387): 1565 - 1575.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
J.-Y. Lee and D.-H. Lee
Use of Serial Analysis of Gene Expression Technology to Reveal Changes in Gene Expression in Arabidopsis Pollen Undergoing Cold Stress
Plant Physiology, June 1, 2003; 132(2): 517 - 529.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
J. P. Hammond, M. J. Bennett, H. C. Bowen, M. R. Broadley, D. C. Eastwood, S. T. May, C. Rahn, R. Swarup, K. E. Woolaway, and P. J. White
Changes in Gene Expression in Arabidopsis Shoots during Phosphate Starvation and the Potential for Developing Smart Plants
Plant Physiology, June 1, 2003; 132(2): 578 - 596.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
N. J. Provart, P. Gil, W. Chen, B. Han, H.-S. Chang, X. Wang, and T. Zhu
Gene Expression Phenotypes of Arabidopsis Associated with Sensitivity to Low Temperatures
Plant Physiology, June 1, 2003; 132(2): 893 - 906.
[Abstract] [Full Text] [PDF]


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Genes Dev.Home page
V. Chinnusamy, M. Ohta, S. Kanrar, B.-h. Lee, X. Hong, M. Agarwal, and J.-K. Zhu
ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis
Genes & Dev., April 15, 2003; 17(8): 1043 - 1054.
[Abstract] [Full Text] [PDF]


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Plant CellHome page
K. E. Vlachonasios, M. F. Thomashow, and S. J. Triezenberg
Disruption Mutations of ADA2b and GCN5 Transcriptional Adaptor Genes Dramatically Affect Arabidopsis Growth, Development, and Gene Expression
PLANT CELL, March 1, 2003; 15(3): 626 - 638.
[Abstract] [Full Text] [PDF]


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Plant Physiol.Home page
L.-X. Yu and T. L. Setter
Comparative Transcriptional Profiling of Placenta and Endosperm in Developing Maize Kernels in Response to Water Deficit
Plant Physiology, February 1, 2003; 131(2): 568 - 582.
[Abstract] [Full Text] [PDF]




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