Specific redox and iron homeostasis responses in the root tip of Arabidopsis upon zinc excess

Abstract

Zinc (Zn) excess negatively impacts primary root growth in Arabidopsis thaliana. Yet, the effects of Zn excess on specific growth processes in the root tip (RT) remain largely unexplored. Transcriptomics, ionomics, and metabolomics were used to examine the specific impact of Zn excess on the RT compared with the remaining root (RR). Zn excess exposure resulted in a shortened root apical meristem and elongation zone, with differentiation initiating closer to the tip of the root. Zn accumulated at a lower concentration in the RT than in the RR. This pattern was associated with lower expression of Zn homeostasis and iron (Fe) deficiency response genes. A distinct distribution of Zn and Fe in RT and RR was highlighted by laser ablation inductively coupled plasma-mass spectrometry analysis. Specialized tryptophan (Trp)-derived metabolism genes, typically associated with redox and biotic stress responses, were specifically upregulated in the RT upon Zn excess, among those Phytoalexin Deficient 3 (PAD3) encoding the last enzyme of camalexin synthesis. In the roots of wild-type seedlings, camalexin concentration increased by sixfold upon Zn excess, and a pad3 mutant displayed increased Zn sensitivity and an altered ionome. Our results indicate that distinct redox and iron homeostasis mechanisms are key elements of the response to Zn excess in the RT.

Keywords: Arabidopsis thaliana; camalexin; iron deficiency; laser ablation ICP‐MS; metal transporter; root apical meristem; specialized metabolism; zinc.