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

Abstract

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.

Pathways of cadmium fluxes in the root of the halophyte Suaeda salsa

“…As a non-essential element, Cd is often assumed to be taken up by transporters for essential elements such as Zn (Pence et al, 2000), Fe (Cohen et al, 1998;Connolly et al, 2002) and Ca (Besson-Bard et al, 2009) as a consequence of a lack of specificity of these transport proteins. Although there have been some reports on Cd 2 þ entry primarily via uptake systems for essential elements, currently it remains unclear as to whether this is also the case for halophyte plants.…”

“…The characteristics of metal transport in the membrane of different plants may not be identical between halophytes and non-halophytes, although some hypotheses have been formulated to explain this process for the latter group of plants. As a non-essential element for plants, cadmium has been assumed to be taken up by transporters for essential elements as a consequence of lack of specificity of the transporters (Pence et al, 2000;Cohen et al, 1998;Connolly et al, 2002;Besson-Bard et al, 2009).…”

Differential effects of nitrogen forms on cell wall phosphorus remobilization in rice (Oryza sativa) are mediated by nitric oxide, pectin content and the expression of the phosphate transporter OsPT2

“…The epifluorescence images were captured by an Eclipse 80i, EX 460-500, DM 505, and BA 510-560 (Nikon, Melville, NY). The fluorescence intensity was measured using Photoshop 7.0 (Adobe Systems, Mountain View, CA) according to Besson-Bard et al (2009).…”

NO and H2O2 contribute to SO2 toxicity via Ca2+ signaling in Vicia faba guard cells

“…SO 2 exposure increased NO and H 2 O 2 levels in V. faba guard cells. Elevated levels of H 2 O 2 and NO can provoke both beneficial and harmful effects in plants responding to abiotic environmental stresses (Besson-Bard et al 2009;Arasimowicz and Floryszak-Wieczorek 2007;Qiao and Fan 2014;Rodríguez-Serrano et al 2012;Jeandroz et al 2013;Yi et al 2014). We have shown previously that an increased H 2 O 2 level mediates SO 2 toxicity in stomatal guard cells of V. faba .…”

“…Hydrogen peroxide (H 2 O 2 ) and NO, which function both synergistically and independently, have been established as ubiquitous signal transduction components to mediate various biological processes, including defense-related gene expression, stomatal closure, and programmed cell death (PCD) (Hausladen and Stamler 1998;Yamasaki and Sakihama 2000;Neill et al 2002;Brüne 2003;Mori and Schroeder 2004;De Pinto et al 2006;Reape and McCabe 2008;Shao et al 2008;Besson-Bard et al 2009;González et al 2012; Responsible editor: Yi-ping Chen Electronic supplementary material The online version of this article (doi:10.1007/s11356-017-8612-6) contains supplementary material, which is available to authorized users. Felicitas et al 2013).…”