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

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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				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]

				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]

				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]

				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]

				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]

				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]

				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]

				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]

				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]

				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]

				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]

				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]

				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]

				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]

				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]