The Receptor-like Cytoplasmic Kinase BIK1 Localizes to the Nucleus and Regulates Defense Hormone Expression during Plant Innate Immunity

Abstract

SUMMARY Plants employ cell-surface pattern recognition receptors (PRRs) to detect pathogens. Although phytohormones produced during PRR signaling play an essential role in innate immunity, a direct link between PRR activation and hormone regulation is unknown. EFR is a PRR that recognizes bacterial EF-Tu and activates immune signaling. Here we report that EFR regulates the phytohormone jasmonic acid (JA) through direct phosphorylation of a receptor-like cytoplasmic kinase, BIK1. The BIK1 structure revealed that the EFR-phosphorylated sites reside on a uniquely extended loop away from the BIK1 kinase core domain. Phosphomimetic mutations of these sites resulted in increased phytohormones and enhanced resistance to bacterial infections. In addition to its documented plasma membrane localization, BIK1 also localizes to the nucleus and interacts directly with WRKY transcription factors involved in the JA and salicylic acid (SA) regulation. These findings demonstrate the mechanistic basis of signal transduction from PRR to phytohormones, mediated through a PRR-BIK1-WRKY axis.

Comparing Arabidopsis receptor kinase and receptor protein‐mediated immune signaling reveals BIK1‐dependent differences

“…Lal et al . () recently reported that, in addition to its known plasma membrane localization, BIK1 also localizes to the nucleus. BIK1 interacts with and phosphorylates transcription factors that are known to be involved in SA and jasmonic acid signaling (WRKY33, 50, and 57) in vitro .…”

The MAP4 Kinase SIK1 Ensures Robust Extracellular ROS Burst and Antibacterial Immunity in Plants

“…Phosphorylated BIK1 was recently demonstrated to be directly involved in regulating levels of the defense hormones JA and SA (Lal et al, 2018). When autoimmune effects are removed, the corresponding genes of some mutants, such as saul1 , have been shown to facilitate immune signaling (Tong et al, 2017).…”

Tyrosine phosphorylation of the lectin receptor‐like kinase LORE regulates plant immunity

“…Many RLCKs phosphorylate downstream immune proteins; for example, upon activation by flg22, BIK1 and PBL1 phosphorylate RbohD at multiple sites required for ROS production (Kadota et al , ; Li et al , ). Following the perception of EF‐Tu, EFR phosphorylates the RLCK BIK1, and the phosphorylated BIK1 localizes to the nucleus to regulate WRKY TF‐mediated immunity (Lal et al , ). During fungal pathogen invasion, the LysM‐RLK LYK5 cooperates with CERK1 to recognize chitin and subsequently activates RLCK VII‐4 subfamily members, which further phosphorylate the MAPK cascade, leading to immune responses (Bi et al , ).…”

“…The Arabidopsis RLCK BOTRYTIS‐INDUCED KINASE1 (BIK1) plays an important role downstream of PRRs. Lal et al () reported that EFR trans‐phosphorylated BIK1 at the S89 and T90 residues and that phosphorylation of these two sites enabled BIK1 to localize to the nucleus and regulate the phosphorylation of WRKY transcription factors (TFs), triggering immune responses. In addition, BIK1 directly interacts with and phosphorylates RBOHD upon PAMP perception, which contributes to plant immunity by controlling the ROS burst and stomatal closure (Kadota et al , ; Li et al , ).…”