Unlocking Nature's Defense: Plant Pattern Recognition Receptors as Guardians Against Pathogenic Threats

Abstract

Embedded in the plasma membrane of plant cells, receptor kinases (RKs) and receptor proteins (RPs) act as key sentinels, responsible for detecting potential pathogenic invaders. These proteins were originally characterized more than three decades ago as disease resistance (R) proteins, a concept that was formulated based on Harold Flor's gene-for-gene theory. This theory implies genetic interaction between specific plant R proteins and corresponding pathogenic effectors, eliciting effector-triggered immunity (ETI). Over the years, extensive research has unraveled their intricate roles in pathogen sensing and immune response modulation. RKs and RPs recognize molecular patterns from microbes as well as dangers from plant cells in initiating pattern-triggered immunity (PTI) and danger-triggered immunity (DTI), which have intricate connections with ETI. Moreover, these proteins are involved in maintaining immune homeostasis and preventing autoimmunity. This review showcases seminal studies in discovering RKs and RPs as R proteins and discusses the recent advances in understanding their functions in sensing pathogen signals and the plant cell integrity and in preventing autoimmunity, ultimately contributing to a robust and balanced plant defense response. [Formula: see text] The author(s) have dedicated the work to the public domain under the Creative Commons CC0 "No Rights Reserved" license by waiving all of his or her rights to the work worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law, 2024.

Keywords: danger-triggered immunity (DTI); effector-triggered immunity (ETI); pathogen infection; pattern-triggered immunity (PTI); plant immunity; receptor kinases (RKs); receptor proteins (RPs).

Fig. 1.

Timeline of the studies of receptor kinases/receptor proteins (RKs/RPs) in plant immunity. Some representative studies of RKs and RPs in plant immunity are chronically highlighted along with identifications of some earliest nucleotide-binding site leucine-rich repeat receptors (NLRs) and R proteins, pathogen elicitors, pathogen-associated molecular patterns (PAMPs)/microbe-associated molecular patterns (MAMPs)/danger-associated molecular patterns (DAMPs)/phytocytokines, and avirulence factors to showcase Flor’s gene-for-gene theory in molecular plantpathogen interaction. Important signaling events and components in pattern-triggered immunity (PTI)/danger-triggered immunity (DTI), structural analyses of RKs/RPs, and models of plant immunity are included to highlight complex mechanisms underlying pathogen recognition and plantpathogen coevolution. Please note that because of space limitations, not all relevant works are mentioned. ADR1, ACTIVATED DISEASE RESISTANCE 1; Avr, avirulence; BAK1, BRASSINOSTEROID-INSENSITIVE 1-ASSOCIATED KINASE 1; BTL2, BAK-TO-LIFE 2; CADL, CANNOT RESPOND TO DMBQ-LIKE PROTEIN; CARD1, CANNOT RESPOND TO DMBQ (2,6-dimethoxy-1,4-benzoquinone) 1; CDPK, calcium-dependent protein kinases; CEBiP, CHITIN ELICITOR-BINDING PROTEIN; CERK1, CHITIN ELICITOR RECEPTOR KINASE 1; Cf-9, Cladosporium fulvum resistance-9; CORE, cold shock protein receptor; CSPR, RECEPTOR-LIKE PROTEIN REQUIRED FOR CSP22 RESPONSIVENESS; CuRe1, CUSCUTA RECEPTOR 1; DORN1, DOES NOT RESPOND TO NUCLEOTIDES; EDS1, ENHANCED DISEASE SUSCEPTIBILITY 1; EFR, EF-Tu RECEPTOR; EIX, ethylene-inducing xylanase; ELR, elicitin response; EPR3, EXOPOLYSACCHARIDE RECEPTOR 3; ETI, effector-triggered immunity; FER, FERONIA; FLS2, FLAGELLIN SENSING 2; FLS3, FLAGELLIN-SENSING 3; HAMP, herbivore-associated molecular pattern; Hcr9-4E, homologues of Cladosporium resistance gene Cf-9 4E; HM1, Helminthosporium carbonum susceptibility 1; HPCA1, HYDROGEN-PEROXIDE-INDUCED Ca²⁺ INCREASES 1; HSL3, HAESA-LIKE 3; INR, inceptin receptor; LecRK, LECTIN RECEPTOR KINASE; LLG2, LORELEI-LIKE-GPI-ANCHORED PROTEIN 2; LORE, LIPOOLIGOSACCHARIDE-SPECIFIC REDUCED ELICITATION; LPS, lipopolysaccharides; LYK, LysM-CONTAINING RECEPTOR-LIKE KINASE; LYK3, LYSIN-MOTIF-RECEPTOR LIKE KINASE 3; LYP, LysM-containing protein; MAPK, mitogen-activated protein kinase; MIK2, LRR-RK MALE DISCOVERER 1-INTERACTING RECEPTOR LIKE KINASE 2; NFP, NOD-FACTOR PERCEPTION; NFR1/NFR5, NOD FACTOR RECEPTORS 1 and 5; NILR1, NEMATODE-INDUCED LRR-RLK 1; NO, nitric oxide; PAD4, PHYTOALEXIN DEFICIENT 4; PEPR1, PEP RECEPTOR 1; PERU, Pep-13 receptor unit; PG, peptidoglycan; PGN, peptidoglycan; RALF, RAPID ALKALINIZATION FACTOR; RaxX, XA21-mediated immunity X; RBOHD, respiratory burst oxidase homolog D; RDA2, RESISTANT TO DFPM-INHIBITION OF ABSCISIC ACID SIGNALING 2; RLCK, receptor-like cytoplasmic kinase; ROS, reactive oxygen species; RPM1, resistance to Pseudomonas syringae pv. maculicola 1; RPS2, RESISTANT TO P. syringae 2; RXEG1, Response to XEG1; SOBIR1, SUPPRESSOR OF BAK1-INTERACTING RECEPTOR-LIKE KINASE 1-1; SYR1/2, SYSTEMIN RECEPTOR 1 and 2; WAK, WALL-ASSOCIATED KINASE; XA21, Xanthomonas oryzae pv. oryzae RESISTANCE 21; XPS1, XANTHINE/PERMEASE SENSING 1.

Fig. 2.

A model of BAK1/BTL2-mediated pattern-triggered immunity (PTI)–danger-triggered immunity (DTI)–effector-triggered immunity (ETI) interaction. When a pathogen invades, PTI serves as the primary defense mechanism against infections, and ETI is activated via the recognition of pathogen effectors by nucleotide-binding site leucine-rich repeat receptors (NLRs). BAK1 is an essential co-receptor of multiple pattern recognition receptors (PRRs) that initiate PTI. Pathogen-induced PTI stimulates the production of modified self-components known as danger-associated molecular patterns (DAMPs) and phytocytokines, which elicit DTI. DTI could amplify PTI and activate ETI to establish robust protection against pathogen infections. Overactivation of ETI could lead to autoimmunity. BAK1 is also essential to keep BTL2 inactive, which otherwise overactivates DTI and ETI. Thus, BAK1 has dual roles in activating PTI and restraining DTI and ETI. Some pathogens could secrete effectors that target BAK1 for degradation or perturbation, which leads to the disruption of PTI. Meanwhile, BTL2 is derepressed in the absence of BAK1, and associates with PRRs or other receptor kinases (RKs) to activate DTI. This activated DTI triggers EDS1-PAD4-ADR1-mediated ETI. It is likely that NLRs, especially TNLs (Toll/interleukin receptor domain-containing NLRs), are involved in the activation of the EDS1-PAD4-ADR1 module. Thus, BTL2-mediated DTI is a double-edged sword, which could compensate for the disrupted PTI when BAK1 is targeted by pathogens, but also could induce autoimmunity when BAK1 and its closest homolog, SERK4, are fully disrupted by pathogens. MAMPs, microbe-associated molecular patterns.