Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation

J Biol Chem. 2008 Apr 4;283(14):8885-92. doi: 10.1074/jbc.M708106200. Epub 2008 Jan 23.

Abstract

Plant respiratory burst oxidase homolog (rboh) proteins, which are homologous to the mammalian 91-kDa glycoprotein subunit of the phagocyte oxidase (gp91(phox)) or NADPH oxidase 2 (NOX2), have been implicated in the production of reactive oxygen species (ROS) both in stress responses and during development. Unlike mammalian gp91(phox)/NOX2 protein, plant rboh proteins have hydrophilic N-terminal regions containing two EF-hand motifs, suggesting that their activation is dependent on Ca(2+). However, the significance of Ca(2+) binding to the EF-hand motifs on ROS production has been unclear. By employing a heterologous expression system, we showed that ROS production by Arabidopsis thaliana rbohD (AtrbohD) was induced by ionomycin, which is a Ca(2+) ionophore that induces Ca(2+) influx into the cell. This activation required a conformational change in the EF-hand region, as a result of Ca(2+) binding to the EF-hand motifs. We also showed that AtrbohD was directly phosphorylated in vivo, and that this was enhanced by the protein phosphatase inhibitor calyculin A (CA). Moreover, CA itself induced ROS production and dramatically enhanced the ionomycin-induced ROS production of AtrbohD. Our results suggest that Ca(2+) binding and phosphorylation synergistically activate the ROS-producing enzyme activity of AtrbohD.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs / physiology
  • Arabidopsis / enzymology*
  • Arabidopsis / genetics
  • Arabidopsis Proteins / biosynthesis*
  • Arabidopsis Proteins / genetics
  • Calcium / metabolism*
  • Enzyme Inhibitors / pharmacology
  • Gene Expression Regulation, Enzymologic / drug effects
  • Gene Expression Regulation, Enzymologic / physiology*
  • Gene Expression Regulation, Plant / drug effects
  • Gene Expression Regulation, Plant / physiology*
  • Hydrophobic and Hydrophilic Interactions
  • Ionomycin / pharmacology
  • Ionophores / pharmacology
  • Marine Toxins
  • Multienzyme Complexes / biosynthesis*
  • Multienzyme Complexes / genetics
  • NADH, NADPH Oxidoreductases / biosynthesis*
  • NADH, NADPH Oxidoreductases / genetics
  • Oxazoles / pharmacology
  • Phosphorylation / drug effects
  • Protein Structure, Tertiary / physiology
  • Reactive Oxygen Species / metabolism*

Substances

  • Arabidopsis Proteins
  • Enzyme Inhibitors
  • Ionophores
  • Marine Toxins
  • Multienzyme Complexes
  • Oxazoles
  • Reactive Oxygen Species
  • Ionomycin
  • calyculin A
  • NADH oxidase
  • NADH, NADPH Oxidoreductases
  • Calcium