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First published online July 13, 2007; 10.1104/pp.107.101808

Plant Physiology 145:174-182 (2007)
© 2007 American Society of Plant Biologists

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PLANTS INTERACTING WITH OTHER ORGANISMS

A Rhizosphere Fungus Enhances Arabidopsis Thermotolerance through Production of an HSP90 Inhibitor1

Catherine A. McLellan2,3, Thomas J. Turbyville2, E.M. Kithsiri Wijeratne, Arthur Kerschen, Elizabeth Vierling, Christine Queitsch4, Luke Whitesell and A.A. Leslie Gunatilaka*

FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138 (C.A.M., C.Q.); Southwest Center for Natural Products Research, Office of Arid Lands Studies, College of Agriculture and Life Sciences, University of Arizona, Tucson, Arizona 85706 (T.J.T., E.M.K.W., A.A.L.G.); Department of Plant Sciences (A.K.) and Department of Biochemistry and Molecular Biophysics (E.V.), University of Arizona, Tucson, Arizona 85721; and Whitehead Institute for Biomedical Research, Cambridge, Massachusetts 02142 (L.W.)

The molecular chaperone HEAT SHOCK PROTEIN90 (HSP90) is essential for the maturation of key regulatory proteins in eukaryotes and for the response to temperature stress. Earlier, we have reported that fungi living in association with plants of the Sonoran desert produce small molecule inhibitors of mammalian HSP90. Here, we address whether elaboration of the HSP90 inhibitor monocillin I (MON) by the rhizosphere fungus Paraphaeosphaeria quadriseptata affects plant HSP90 and plant environmental responsiveness. We demonstrate that MON binds Arabidopsis (Arabidopsis thaliana) HSP90 and can inhibit the function of HSP90 in lysates of wheat (Triticum aestivum) germ. MON treatment of Arabidopsis seedlings induced HSP101 and HSP70, conserved components of the stress response. Application of MON, or growth in the presence of MON, allowed Arabidopsis wild type but not AtHSP101 knockout mutant seedlings to survive otherwise lethal temperature stress. Finally, cocultivation of P. quadriseptata with Arabidopsis enhanced plant heat stress tolerance. These data demonstrate that HSP90-inhibitory compounds produced by fungi can influence plant growth and responses to the environment.

1 This work was supported in part by the U.S. National Institutes of Health (grant no. R01–CA090265 to A.A.L.G. and grant no. R21–CA091056 to L.W.) and by the U.S. Department of Energy (Energy Biosciences Program grant no. DE–RG03–99ER20338 to E.V.). Fellowship support of T.J.T. was provided by the University of Arizona Bio5 Institute.

2 These authors contributed equally to the article.

3 Present address: Whitehead Institute for Biomedical Research, Cambridge, MA 02142.

4 Present address: Department of Genome Sciences, University of Washington, Seattle, WA 98195.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: A.A. Leslie Gunatilaka (leslieg{at}ag.arizona.edu).

www.plantphysiol.org/cgi/doi/10.1104/pp.107.101808

* Corresponding author; e-mail leslieg{at}ag.arizona.edu.

Received May 4, 2007; accepted June 6, 2007; published July 13, 2007.




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