4.7 Article

PDX1.1-dependent biosynthesis of vitamin B6 protects roots from ammonium-induced oxidative stress

Journal

MOLECULAR PLANT
Volume 15, Issue 5, Pages 820-839

Publisher

CELL PRESS
DOI: 10.1016/j.molp.2022.01.012

Keywords

ammonium nutrition; apoplastic pH; Fe mobilization; root elongation; pyridoxine; ROS scavenging

Funding

  1. Deutsche Forschungsgemeinschaft (Germany) [WI1728/13-2]
  2. Swiss National Science Foundation [31003A_14117, IZLIZ3_183193]
  3. Swiss National Science Foundation (SNF) [IZLIZ3_183193] Funding Source: Swiss National Science Foundation (SNF)

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This study found that apoplastic acidification induced by ammonium is associated with iron precipitation and hydrogen peroxide accumulation along the stele in root tips, indicating iron-dependent ROS formation. Through screening ammonium sensitivity in genes, PDX1.1 was identified as an ammonium-responsive gene that is upregulated in the root stele and catalyzes the de novo synthesis of vitamin B-6. Mutants of pdx1.1 exhibit hypersensitivity to ammonium, while chemical complementation or overexpression of PDX1.1 restores root elongation. The synthesis of non-phosphorylated B-6 vitamers mediated by PDX1.1 acts as a primary strategy to protect roots from ammonium-induced ROS formation.
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 B-6. 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 B-6 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 B-6 vitamers acts as a primary strategy to protect roots from ammonium-dependent ROS formation.

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