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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Nitric Oxide Contributes to Cadmium Toxicity in Arabidopsis by Promoting Cadmium Accumulation in Roots and by Up-Regulating Genes Related to Iron Uptake^1,[W]

UMR INRA 1088/CNRS 5184/Université de Bourgogne, Plante-Microbe-Environnement, 21065 Dijon cedex, France (A.B.-B., A.P., D.W.); UMR 118 Amélioration des Plantes et Biotechnologies Végétales, INRA/Agrocampus Rennes/Université Rennes 1, 35653 Le Rheu cedex, France (A.G.); Laboratoire de Bioénergétique et Biotechnologie des Bactéries et Microalgues, SBVME, IBEB, DSV, CEA, CNRS, Université Aix Marseille, 13108 Saint Paul lez Durance, France (P.R., P.A.); Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, UMR 5004 Agro-M/CNRS/INRA/UMII, 34060 Montpellier cedex 1, France (C.D., F.G.); and Unité de Recherche en Génomique Végétale, UMR 8114 CNRS/INRA/Université d'Evry-Val d'Essonne, 91057 Evry, France (L.T., J.-P.R.)

Nitric oxide (NO) functions as a cell-signaling molecule in plants. In particular, a role for NO in the regulation of iron homeostasis and in the plant response to toxic metals has been proposed. Here, we investigated the synthesis and the role of NO in plants exposed to cadmium (Cd²⁺), a nonessential and toxic metal. We demonstrate that Cd²⁺ induces NO synthesis in roots and leaves of Arabidopsis (Arabidopsis thaliana) seedlings. This production, which is sensitive to NO synthase inhibitors, does not involve nitrate reductase and AtNOA1 but requires IRT1, encoding a major plasma membrane transporter for iron but also Cd²⁺. By analyzing the incidence of NO scavenging or inhibition of its synthesis during Cd²⁺ treatment, we demonstrated that NO contributes to Cd²⁺-triggered inhibition of root growth. To understand the mechanisms underlying this process, a microarray analysis was performed in order to identify NO-modulated root genes up- and down-regulated during Cd²⁺ treatment. Forty-three genes were identified encoding proteins related to iron homeostasis, proteolysis, nitrogen assimilation/metabolism, and root growth. These genes include IRT1. Investigation of the metal and ion contents in Cd²⁺-treated roots in which NO synthesis was impaired indicates that IRT1 up-regulation by NO was consistently correlated to NO's ability to promote Cd²⁺ accumulation in roots. This analysis also highlights that NO is responsible for Cd²⁺-induced inhibition of root Ca²⁺ accumulation. Taken together, our results suggest that NO contributes to Cd²⁺ toxicity by favoring Cd²⁺ versus Ca²⁺ uptake and by initiating a cellular pathway resembling those activated upon iron deprivation.

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 Wendehenne (wendehen{at}dijon.inra.fr).

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

www.plantphysiol.org/cgi/doi/10.1104/pp.108.133348

^* Corresponding author; e-mail wendehen{at}dijon.inra.fr.

Received November 27, 2008; accepted January 20, 2009; published January 23, 2009.

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