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

Yasuhiro Kadota; Jan Sklenar; Paul Derbyshire; Lena Stransfeld; Shuta Asai; Vardis Ntoukakis; Jonathan Dg Jones; Ken Shirasu; Frank Menke; Alexandra Jones; Cyril Zipfel

doi:10.1016/j.molcel.2014.02.021

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.

Authors

Affiliations

¹ The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, UK; RIKEN Center for Sustainable Resource Science, Plant Immunity Research Group, Suehiro-cho 1-7-22 Tsurumi-ku, Yokohama 230-0045, Japan.
² The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, UK.
³ RIKEN Center for Sustainable Resource Science, Plant Immunity Research Group, Suehiro-cho 1-7-22 Tsurumi-ku, Yokohama 230-0045, Japan.
⁴ The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, UK. Electronic address: [email protected].

PMID: 24630626
DOI: 10.1016/j.molcel.2014.02.021

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*
Nicotiana / enzymology*
Nicotiana / genetics
Nicotiana / immunology
Nicotiana / microbiology
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

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

Abstract

Publication types

MeSH terms

Substances

Grants and funding