Abstract
Despite serving as a major inorganic nitrogen source for plants, ammonium causes toxicity at elevated concentrations, inhibiting root elongation early on. While previous studies have shown that ammonium-inhibited root development relates to ammonium uptake and formation of reactive oxygen species (ROS) in roots, it remains unclear about the mechanisms underlying the repression of root growth and how plants cope with this inhibitory effect of ammonium. In this study, we demonstrate that ammonium-induced apoplastic acidification co-localizes with Fe precipitation and hydrogen peroxide (H2O2) accumulation along the stele of the elongation and differentiation zone in root tips, indicating Fe-dependent ROS formation. By screening ammonium sensitivity in T-DNA insertion lines of ammonium-responsive genes, we identified PDX1.1, which is upregulated by ammonium in the root stele and whose product catalyzes de novo biosynthesis of vitamin B6. Root growth of pdx1.1 mutants is hypersensitive to ammonium, while chemical complementation or overexpression of PDX1.1 restores root elongation. This salvage strategy requires non-phosphorylated forms of vitamin B6 that are able to quench ROS and rescue root growth from ammonium inhibition. Collectively, these results suggest that PDX1.1-mediated synthesis of non-phosphorylated B6 vitamers acts as a primary strategy to protect roots from ammonium-dependent ROS formation.
Highlights
Nitrogen (N) is an essential mineral element for plant development and is extensively applied in crop production (Xu et al, 2012)
Application of ammonium-based N fertilizers in agricultural plant production bears the risk of impaired root development when roots are exposed to ammonium-rich soil patches (Britto and Kronzucker, 2002; Watt et al, 2006)
Plants have evolved several strategies to cope with the adverse effects of predominant ammonium nutrition, which comprise enhanced N assimilation in roots (Cruz et al, 2006; Guan et al, 2016; Konishi et al, 2017), ammonium compartmentalization to the apoplast or vacuole (Loqueet al., 2005; Li et al, 2010; Bai et al, 2014), and activation of enzymatic anti-oxidation systems to cope with ammonium-triggered reactive oxygen species (ROS) production (Patterson et al, 2010; Xie et al, 2015)
Summary
Nitrogen (N) is an essential mineral element for plant development and is extensively applied in crop production (Xu et al, 2012). Ammonium is a preferential inorganic N source for many plant species (Gazzarrini et al, 1999), excessive ammonium causes toxicity resulting in leaf chlorosis and suppressed root growth (Britto and Kronzucker, 2002). These symptoms rely on ammonium triggering multiple physiological and morphological responses, including changes in apoplastic and cytosolic pH, gene expression, protein modification, ion transport, N metabolism, redox and phytohormone status, and root system architecture
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