Cadmium (Cd) is a toxic element and a widespread health hazard. Preventing its entry into crops is an outstanding issue. 3,4-Dihydroxy-L-phenylalanine (L-DOPA) is a non-proteinogenic amino acid that is secreted by a few legume plants and affects neighboring plants. Exogenous L-DOPA triggers iron (Fe) uptake by roots of Arabidopsis thaliana Columbia-0 ecotype through transcriptional activation of Fe deficiency genes, including IRONMANs (IMAs), which encode peptides regulating Fe homeostasis. Ectopic expression of IRONMAN1 was reported to enhance Cd tolerance in Arabidopsis. We therefore hypothesized that L-DOPA could also enhance Cd tolerance by stimulating the expression of IMAs. In the present study, the elemental profile and the expression of key genes of plants exposed to a combination of Cd and L-DOPA were studied. The results show that exogenous L-DOPA considerably enhances the Cd tolerance of Arabidopsis thaliana, abolishing the Cd-induced chlorosis and necrosis, and reducing Cd accumulation. This increased tolerance is not due to an enhanced Fe uptake and is not mediated by IMAs. Instead, L-DOPA triggered a peculiar transcriptional program that led to an increased expression of a branch of the Fe deficiency pathway comprising the transcription factor bHLH39 but, surprisingly, not its target genes FRO2 and IRT1. The NICOTIANAMINE SYNTHASE 4 (NAS4) gene, which mediates Cd tolerance, was highly and specifically upregulated by the application of L-DOPA and Cd combined. These results suggest that Fe homeostasis is controlled by small molecules through currently unknown mechanisms that could be leveraged to manipulate Fe and Cd accumulation in plants.
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