Nitric Oxide Contributes to Cadmium Toxicity in Arabidopsis by Promoting Cadmium Accumulation in Roots and by Up-Regulating Genes Related to Iron Uptake

• Published in: Plant physiology (Bethesda) Vol. 149; no. 3; pp. 1302 - 1315
• Main Authors: Besson-Bard, Angélique, Gravot, Antoine, Richaud, Pierre, Auroy, Pascaline, Duc, Céline, Gaymard, Frédéric, Taconnat, Ludivine, Renou, Jean-Pierre, Pugin, Alain, Wendehenne, David
• Format: Journal Article
• Language: English
• Published: Rockville, MD American Society of Plant Biologists 01.03.2009; Oxford University Press ; American Society of Plant Biologists
• Subjects: Arabidopsis - drug effects; Arabidopsis - genetics; Biological and medical sciences; Cadmium; Cadmium - metabolism; Cadmium - toxicity; Environmental Stress and Adaptation to Stress; Fluorescence; Fundamental and applied biological sciences. Psychology; Gene Expression Regulation, Plant - drug effects; Genes; Genes, Plant; Iron; Iron - metabolism; Leaves; Life Sciences; Models, Biological; NG-Nitroarginine Methyl Ester - pharmacology; Nitric Oxide - biosynthesis; Nitric Oxide - metabolism; Oxides; Plant cells; Plant Leaves - drug effects; Plant Leaves - genetics; Plant Leaves - metabolism; Plant physiology and development; Plant roots; Plant Roots - cytology; Plant Roots - genetics; Plant Roots - growth & development; Plant Roots - metabolism; Plants; Root growth; Up-Regulation - drug effects; Vegetal Biology; Cadmium; Root; Toxicity; Iron; Heavy metal; Arabidopsis thaliana; Absorption; Gene; Plant physiology; Cruciferae; Dicotyledones; Nitric oxide; Angiospermae; Spermatophyta; Experimental plant; iron homeostasis; Arabidopsis; AtNOA1; plasma membrane transporter; cadmium; roots; toxic metals
• ISSN: 0032-0889; 1532-2548; 1532-2548
• DOI: 10.1104/pp.108.133348

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.