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J. Biol. Chem., Vol. 281, Issue 37, 27557-27565, September 15, 2006

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Structural Basis for the Redox Control of Plant Glutamate Cysteine Ligase^*

Michael Hothorn¹, Andreas Wachter, Roland Gromes, Tobias Stuwe, Thomas Rausch, and Klaus Scheffzek²

From the Structural and Computational Biology Unit, European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg and the Department of Molecular Ecophysiology, Heidelberg Institute for Plant Sciences, Im Neuenheimer Feld 360, 69120 Heidelberg, Germany

Glutathione (GSH) plays a crucial role in plant metabolism and stress response. The rate-limiting step in the biosynthesis of GSH is catalyzed by glutamate cysteine ligase (GCL) the activity of which is tightly regulated. The regulation of plant GCLs is poorly understood. The crystal structure of substrate-bound GCL from Brassica juncea at 2.1-Å resolution reveals a plant-unique regulatory mechanism based on two intramolecular redox-sensitive disulfide bonds. Reduction of one disulfide bond allows a -hairpin motif to shield the active site of B. juncea GCL, thereby preventing the access of substrates. Reduction of the second disulfide bond reversibly controls dimer to monomer transition of B. juncea GCL that is associated with a significant inactivation of the enzyme. These regulatory events provide a molecular link between high GSH levels in the plant cell and associated down-regulation of its biosynthesis. Furthermore, known mutations in the Arabidopsis GCL gene affect residues in the close proximity of the active site and thus explain the decreased GSH levels in mutant plants. In particular, the mutation in rax1-1 plants causes impaired binding of cysteine.

Received for publication, March 23, 2006 , and in revised form, June 8, 2006.

The atomic coordinates and structure factors (code 2GWC and 2GWD) have been deposited in the Protein Data Bank, Research Collaboratory for Structural Bioinformatics, Rutgers University, New Brunswick, NJ (http://www.rcsb.org/).

^* This project was supported in part by the Deutsche Forschungsgemeinschaft (to T. R. and K. S.), by the KWS Saat AG, Einbeck, Germany, and by the Suedzucker AG, Mannheim, Germany (to T. R.). 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 Figs. S1-S4.

¹ Supported by the Peter and Traudl Engelhorn Foundation, Penzberg, Germany.

² To whom correspondence should be addressed. Tel.: 49-(0)6221-387-401; Fax: 49-(0)6221-387-519; E-mail: scheffzek{at}embl.de.

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