Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity

Mol Cell. 2014 Apr 10;54(1):43-55. doi: 10.1016/j.molcel.2014.02.021. Epub 2014 Mar 12.

Abstract

The rapid production of reactive oxygen species (ROS) burst is a conserved signaling output in immunity across kingdoms. In plants, perception of pathogen-associated molecular patterns (PAMPs) by surface-localized pattern recognition receptors (PRRs) activates the NADPH oxidase RBOHD by hitherto unknown mechanisms. Here, we show that RBOHD exists in complex with the receptor kinases EFR and FLS2, which are the PRRs for bacterial EF-Tu and flagellin, respectively. The plasma-membrane-associated kinase BIK1, which is a direct substrate of the PRR complex, directly interacts with and phosphorylates RBOHD upon PAMP perception. BIK1 phosphorylates different residues than calcium-dependent protein kinases, and both PAMP-induced BIK1 activation and BIK1-mediated phosphorylation of RBOHD are calcium independent. Importantly, phosphorylation of these residues is critical for the PAMP-induced ROS burst and antibacterial immunity. Our study reveals a rapid regulatory mechanism of a plant RBOH, which occurs in parallel with and is essential for its paradigmatic calcium-based regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Arabidopsis / enzymology*
  • Arabidopsis / genetics
  • Arabidopsis / immunology
  • Arabidopsis / microbiology
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / immunology*
  • Arabidopsis Proteins / metabolism*
  • Cell Line
  • Enzyme Activation
  • Flagellin / immunology
  • Flagellin / metabolism
  • Gene Expression Regulation, Enzymologic
  • Gene Expression Regulation, Plant
  • Immunity, Innate*
  • Ligands
  • Molecular Sequence Data
  • Multienzyme Complexes
  • NADPH Oxidases / genetics
  • NADPH Oxidases / immunology*
  • Peptide Elongation Factor Tu / immunology
  • Peptide Elongation Factor Tu / metabolism
  • Phosphorylation
  • Plant Immunity*
  • Plant Stomata / immunology
  • Plant Stomata / metabolism
  • Protein Kinases / immunology
  • Protein Kinases / metabolism
  • Protein-Serine-Threonine Kinases / genetics
  • Protein-Serine-Threonine Kinases / metabolism*
  • Reactive Oxygen Species / metabolism
  • Receptors, Immunologic / metabolism
  • Receptors, Pattern Recognition / immunology
  • Receptors, Pattern Recognition / metabolism
  • Signal Transduction
  • Tobacco / enzymology*
  • Tobacco / genetics
  • Tobacco / immunology
  • Tobacco / microbiology

Substances

  • Arabidopsis Proteins
  • EFR protein, Arabidopsis
  • Ligands
  • Multienzyme Complexes
  • Reactive Oxygen Species
  • Receptors, Immunologic
  • Receptors, Pattern Recognition
  • Flagellin
  • respiratory burst oxidase homolog D, Arabidopsis
  • NADPH Oxidases
  • Protein Kinases
  • FLS2 protein, Arabidopsis
  • BIK1 protein, Arabidopsis
  • Protein-Serine-Threonine Kinases
  • Peptide Elongation Factor Tu