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J. Biol. Chem., Vol. 282, Issue 52, 37794-37804, December 28, 2007

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Cytosolic HSP90 Regulates the Heat Shock Response That Is Responsible for Heat Acclimation in Arabidopsis thaliana^*

Kenji Yamada, Yoichiro Fukao, Makoto Hayashi, Mitsue Fukazawa, Iku Suzuki, and Mikio Nishimura¹

From the Department of Cell Biology, National Institute for Basic Biology, Nishigo-naka 38, Myodaiji, Okazaki 444-8585, Aichi, Japan and the Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0101, Japan

Plant survival requires the ability to acclimate to heat. When plants are subjected to heat shock, the expression of various genes is induced, and the plants become tolerant of higher temperatures. We found that transient treatment with geldanamycin and radicicol, two heat shock protein 90 (HSP90) inhibitors, induced heat-inducible genes and heat acclimation in Arabidopsis thaliana seedlings. Heat shock reduced the activity of exogenously expressed glucocorticoid receptor (GR). Since GR activity depends on HSP90, this suggests that heat shock reduces cytosolic HSP90 activity in vivo. Microarray analysis revealed that many of the genes that are up-regulated by both heat shock and HSP90 inhibitors are involved in protein folding and degradation, suggesting that the activation of a protein maintenance system is a crucial part of this response. Most of these genes have heat shock response element-like motifs in their promoters, which suggests that heat shock transcription factor (HSF) is involved in the response to HSP90 inhibition. Several HSF genes are expressed constitutively in A. thaliana, including AtHsfA1d. Recombinant AtHsfA1d protein recognizes the heat shock response element motif and interacts with A. thaliana cytosolic HSP90, HSP90.2. Overexpression of a dominant negative form of HSP90.2 induced the heat-inducible gene. Thus, it appears that in the absence of heat shock, cytosolic HSP90 negatively regulates heat-inducible genes by actively suppressing HSF function. Upon heat shock, cytosolic HSP90 is transiently inactivated, which may lead to HSF activation.

Received for publication, August 27, 2007 , and in revised form, October 4, 2007.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) E-ATMX-12.

^* This work was supported by Ministry of Education, Science, Sports and Culture of Japan Grants-in-Aid 19770040 (to K. Y.) and 16085209 (to M. N.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Tables S1-S5.

¹ To whom correspondence should be addressed: Dept. of Cell Biology, National Institute for Basic Biology, Nishigo-Naka 38, Myodaiji, Okazaki, Aichi 444-8585, Japan. Fax: 81-564-55-7505; E-mail: mikosome{at}nibb.ac.jp.

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