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BIOCHEMICAL PROCESSES AND MACROMOLECULAR STRUCTURES

Poplar Peroxiredoxin Q. A Thioredoxin-Linked Chloroplast Antioxidant Functional in Pathogen Defense¹

Unité Mixte de Recherche Institut National de la Recherche Agronomique-Université Henri Poincaré 1136, Interactions Arbres/Micro-Organismes, Université Henri Poincaré, Faculté des Sciences, BP 239, 54506 Vandoeuvre cedex France (N.R., E.G., M.-N.J., E.D.F., S.D., F.M., J.-P.J.); Institut de Biologie Moléculaire des Plantes, Centre National de la Recherche Scientifique, 67084 Strasbourg cedex France (J.M.G.); Department of Chemistry and Biochemistry, and Center for Biotechnology and Genomics, Texas Tech University, Lubbock, Texas 79409-1061 (M.H., D.B.K.); Institut de Biotechnologie des Plantes, Université de Paris Sud, 91405 Orsay cedex France (S.D.L.); Institut National de la Recherche Agronomique, Unité Pathologie Forestière, F-54280 Seichamps, France (P.F.); and Laboratoire de Biochimie Végétale, CH-2007 Neuchâtel, Switzerland (W.M.)

Peroxiredoxins are ubiquitous thioredoxin- or glutaredoxin-dependent peroxidases, the function of which is to destroy peroxides. Peroxiredoxin Q, one of the four plant subtypes, is a homolog of the bacterial bacterioferritin comigratory proteins. We show here that the poplar (Populus tremula x Populus tremuloides) protein acts as a monomer with an intramolecular disulfide bridge between two conserved cysteines. A wide range of electron donors and substrates was tested. Unlike type II peroxiredoxin, peroxiredoxin Q cannot use the glutaredoxin or cyclophilin isoforms tested, but various cytosolic, chloroplastic, and mitochondrial thioredoxins are efficient electron donors with no marked specificities. The redox midpoint potential of the peroxiredoxin Q catalytic disulfide is -325 mV at pH 7.0, explaining why the wild-type protein is reduced by thioredoxin but not by glutaredoxin. Additional evidence that thioredoxin serves as a donor comes from the formation of heterodimers between peroxiredoxin Q and monocysteinic mutants of spinach (Spinacia oleracea) thioredoxin m. Peroxiredoxin Q can reduce various alkyl hydroperoxides, but with a better efficiency for cumene hydroperoxide than hydrogen peroxide and tertiary butyl hydroperoxide. The use of immunolocalization and of a green fluorescence protein fusion construct indicates that the transit sequence efficiently targets peroxiredoxin Q to the chloroplasts and especially to those of the guard cells. The expression of this protein and of type II peroxiredoxin is modified in response to an infection by two races of Melampsora larici-populina, the causative agent of the poplar rust. In the case of an hypersensitive response, the peroxiredoxin expression increased, whereas it decreased during a compatible interaction.

¹ This work was supported by The Robert A. Welch Foundation (grant no. D-0710 to D.B.K.).

^* Corresponding author; e-mail j2p{at}scbiol.uhp-nancy.fr.

Received November 7, 2003; returned for revision December 2, 2003; accepted December 4, 2003.

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