Receptor Kinases in Plant-Pathogen Interactions: More Than Pattern Recognition

Abstract

Receptor-like kinases (RLKs) and Receptor-like proteins (RLPs) play crucial roles in plant immunity, growth, and development. Plants deploy a large number of RLKs and RLPs as pattern recognition receptors (PRRs) that detect microbe- and host-derived molecular patterns as the first layer of inducible defense. Recent advances have uncovered novel PRRs, their corresponding ligands, and mechanisms underlying PRR activation and signaling. In general, PRRs associate with other RLKs and function as part of multiprotein immune complexes at the cell surface. Innovative strategies have emerged for the rapid identification of microbial patterns and their cognate PRRs. Successful pathogens can evade or block host recognition by secreting effector proteins to "hide" microbial patterns or inhibit PRR-mediated signaling. Furthermore, newly identified pathogen effectors have been shown to manipulate RLKs controlling growth and development by mimicking peptide hormones of host plants. The ongoing studies illustrate the importance of diverse plant RLKs in plant disease resistance and microbial pathogenesis.

Figure 1.

Ligand-Induced Heterodimerization between LRR-RKs and SERKs. Structural alignment of FLS2-flg22-BAK1, PEPR1-Pep1, PXY-TDIF-SERK2, and HAESA-IDA-SERK1 complexes. The structure of FLS2 ECD was used as the template for the alignment. Note that only ECDs were included in the structural studies. N and C denote N and C termini of LRR-RK ECDs and peptides.

Figure 2.

RLCKs Differentially Mediate Immune Signaling from Different PRRs. Different RLCKs known to interact with PRRs are colored in blue. BIK1 and PBL1 directly interact with multiple PRRs or coreceptors, including LRR-RKs (FLS2, EFR, and PEPRs), LRR-RLK (BAK1), and LysM-RLK (CERK1), to mediate immune signaling. The RLCK PBL27 was reported to specifically associate with CERK1 to mediate chitin-triggered immune signaling. In addition, the RLCKs BSK1 and PCRKs are also capable of interacting with FLS2 to mediate flagellin-triggered immune signaling. The rice RLCK185 directly interacts with CERK1 to mediate chitin-triggered signaling. FLS2, EFR, and PEPRs perceive bacteria flagellin, EF-Tu, and endogenous DAPMP Peps, respectively, and recruit coreceptors BAK1/SERKs to form active receptor complexes, whereas the rice LysM-RLP CEBiP and Arabidopsis LysM-RK LYK5 bind chitin and recruit LysM-RLK CERK1 to form active receptor complexes. The activated receptor complexes phosphorylate RLCKs to activate downstream signaling.

Figure 3.

RLCKs Differentially Regulate Downstream Signaling. RLCKs including BIK1, PBL1, RIPK, PCRKs, BSK1, and PBL27 are colored in blue. BIK1 and PBL1 positively regulate multiple downstream responses including RbohD-dependent ROS burst, [Ca²⁺]_cyt increase, and activation of heterotrimeric G proteins. BIK1 and RIPK are required for phosphorylating distinct residues in RIN4, a plasma membrane proton ATPase-interacting protein, to positively or negatively regulate immunity. Proton efflux further regulates other ion channels, such as K⁺ channels. BSK1 positively regulates the ROS burst downstream of FLS2. PCRKs positively regulate SA biosynthesis upon flg22 treatment. PBL27 positively regulates MAPKKK5 to specifically mediate chitin-triggered MPK activation. The activation of RbohD also requires [Ca²⁺]_cyt increase and CPK5. Solid lines indicate direct phosphorylations or protein-protein interactions, whereas dashed lines indicate that direct interactions/phosphorylations are unknown. Arrows indicate positive regulation, while T-bars indicate inhibition.

Figure 4.

Pathogen Effector Proteins Enhance Susceptibility by Interfering with PRR-Mediated Signaling or Mimicking Peptide Hormones. Different effectors and molecular patterns are colored in purple. The fungal apoplastic effectors ECP6 and SLP1 compete with plant receptors for chitin binding. Bacterial cytoplasmic effectors can block PRR-mediated signaling by physically inhibiting (AvrPto and AvrPtoB) or dephosphorylating (HopAO1) PRR kinases, proteolysis of coreceptors (HopB1), proteolysis (AvrPphB) or uridylylation (AvrAC) of RLCKs, ADP-ribosylation of MAPKK or BAK1 (HopF2), or dephosphorylation of MPKs (HopAI1). AvrB induces phosphorylation of RIN4 to stimulate plasma membrane proton ATPase activity. Fungal apoplastic effector F-RALF mimics plant RALF peptide to induce the FER-mediated signaling pathway, which inhibits PRR-specified immunity through crosstalk. The bacterial protein RaxX may mimic plant peptide PSY1 to stimulate PSY1R-mediated signaling, which is known to inhibit PRR-mediated immunity.