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BIOCHEMICAL PROCESSES AND MACROMOLECULAR STRUCTURES

A -Glutamyl Transpeptidase-Independent Pathway of Glutathione Catabolism to Glutamate via 5-Oxoproline in Arabidopsis^1,[W],[OA]

Department of Genetics, Development, and Cell Biology, Iowa State University, Ames, Iowa 50011 (N.O.-O., D.J.O.); RIKEN Plant Science Center, Yokohama 230–0045, Japan (N.O.-O., A.O., K.S.); and School of Life Sciences, University of Science and Technology of China, Hefei, Auhui 230027, China (P.Z., C.X.)

The degradation pathway of glutathione (GSH) in plants is not well understood. In mammals, GSH is predominantly metabolized through the -glutamyl cycle, where GSH is degraded by the sequential reaction of -glutamyl transpeptidase (GGT), -glutamyl cyclotransferase, and 5-oxoprolinase to yield glutamate (Glu) and dipeptides that are subject to peptidase action. In this study, we examined if GSH is degraded through the same pathway in Arabidopsis (Arabidopsis thaliana) as occurs in mammals. In Arabidopsis, the oxoprolinase knockout mutants (oxp1-1 and oxp1-2) accumulate more 5-oxoproline (5OP) and less Glu than wild-type plants, suggesting substantial metabolite flux though 5OP and that 5OP is a major contributor to Glu steady-state levels. In the ggt1-1/ggt4-1/oxp1-1 triple mutant with no GGT activity in any organs except young siliques, the 5OP concentration in leaves was not different from that in oxp1-1, suggesting that GGTs are not major contributors to 5OP production in Arabidopsis. 5OP formation strongly tracked the level of GSH in Arabidopsis plants, suggesting that GSH is the precursor of 5OP in a GGT-independent reaction. Kinetics analysis suggests that -glutamyl cyclotransferase is the major source of GSH degradation and 5OP formation in Arabidopsis. This discovery led us to propose a new pathway for GSH turnover in plants where GSH is converted to 5OP and then to Glu by the combined action of -glutamyl cyclotransferase and 5-oxoprolinase in the cytoplasm.

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: David J. Oliver (doliver{at}iastate.edu).

^[W] The online version of this article contains Web-only data.

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www.plantphysiol.org/cgi/doi/10.1104/pp.108.125716

^* Corresponding author; e-mail doliver{at}iastate.edu.

Received July 3, 2008; accepted August 29, 2008; published September 3, 2008.