Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake.
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 (Cd(2+)), a nonessential and toxic metal. We demonstrate that Cd(2+) 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 Cd(2+). By analyzing the incidence of NO scavenging or inhibition of its synthesis during Cd(2+) treatment, we demonstrated that NO contributes to Cd(2+)-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 Cd(2+) 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 Cd(2+)-treated roots in which NO synthesis was impaired indicates that IRT1 up-regulation by NO was consistently correlated to NO's ability to promote Cd(2+) accumulation in roots. This analysis also highlights that NO is responsible for Cd(2+)-induced inhibition of root Ca(2+) accumulation. Taken together, our results suggest that NO contributes to Cd(2+) toxicity by favoring Cd(2+) versus Ca(2+) uptake and by initiating a cellular pathway resembling those activated upon iron deprivation.
Besson-Bard
Angélique
A
UMR INRA 1088/CNRS 5184/Université de Bourgogne, Plante-Microbe-Environnement, 21065 Dijon cedex, France.
Gravot
Antoine
A
Richaud
Pierre
P
Auroy
Pascaline
P
Duc
Céline
C
Gaymard
Frédéric
F
Taconnat
Ludivine
L
Renou
Jean-Pierre
JP
Pugin
Alain
A
Wendehenne
David
D
D017360:Arabidopsis / Q000187:drug effects* / Q000235:genetics*; D002104:Cadmium / Q000378:metabolism / Q000633:toxicity*; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D017343:Genes, Plant; D007501:Iron / Q000378:metabolism*; D008954:Models, Biological; D019331:NG-Nitroarginine Methyl Ester / Q000494:pharmacology; D009569:Nitric Oxide / Q000096:biosynthesis / Q000378:metabolism*; D018515:Plant Leaves / Q000187:drug effects / Q000235:genetics / Q000378:metabolism; D018517:Plant Roots / Q000166:cytology / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D015854:Up-Regulation / Q000187:drug effects*
D002104:Cadmium; D009569:Nitric Oxide; D007501:Iron; D019331:NG-Nitroarginine Methyl Ester