The EDS1–PAD4–ADR1 node mediates Arabidopsis pattern-triggered immunity

Abstract

Plants deploy cell-surface and intracellular leucine rich-repeat domain (LRR) immune receptors to detect pathogens 1 . LRR receptor kinases and LRR receptor proteins at the plasma membrane recognize microorganism-derived molecules to elicit pattern-triggered immunity (PTI), whereas nucleotide-binding LRR proteins detect microbial effectors inside cells to confer effector-triggered immunity (ETI). Although PTI and ETI are initiated in different host cell compartments, they rely on the transcriptional activation of similar sets of genes 2 , suggesting pathway convergence upstream of nuclear events. Here we report that PTI triggered by the Arabidopsis LRR receptor protein RLP23 requires signalling-competent dimers of the lipase-like proteins EDS1 and PAD4, and of ADR1 family helper nucleotide-binding LRRs, which are all components of ETI. The cell-surface LRR receptor kinase SOBIR1 links RLP23 with EDS1, PAD4 and ADR1 proteins, suggesting the formation of supramolecular complexes containing PTI receptors and transducers at the inner side of the plasma membrane. We detected similar evolutionary patterns in LRR receptor protein and nucleotide-binding LRR genes across Arabidopsis accessions; overall higher levels of variation in LRR receptor proteins than in LRR receptor kinases are consistent with distinct roles of these two receptor families in plant immunity. We propose that the EDS1-PAD4-ADR1 node is a convergence point for defence signalling cascades, activated by both surface-resident and intracellular LRR receptors, in conferring pathogen immunity.Arabidopsis thaliana (hereafter Arabidopsis) cell-surface LRR receptor kinases (LRR-RKs) and LRR receptor protein (LRR-RP)-SOBIR1 complexes recruit the co-receptor BAK1 and signal through receptor-like cytoplasmic kinases (RLCKs) to elicit PTI 3 . Intracellular coiled-coil (CC)-nucleotide-binding LRR (NLR) or TOLL-INTERLEUKIN 1 RECEP-TOR (TIR)-NLR receptors 4 require ADR1-type and NRG1-type helper NLRs (hNLRs) and the lipase-like EDS1 family proteins EDS1, PAD4 and SAG101 to confer ETI 5,6 . While the defence outputs for PTI and ETI are qualitatively similar 2 , where and how pathways activated in different cell compartments converge remain unclear. Effective plant defence relies on mutual potentiation of PTI and ETI pathways 7,8 , suggesting mechanistic links between these two tiers of the plant immune system. RLCKs PBL30 and PBL31 mediate PTIThe Arabidopsis class VII RLCK (RLCK-VII) BIK1 promotes LRR-RK-mediated PTI but is a negative regulator of LRR-RP-mediated PTI 9 . To identify RLCK-VII members with positive roles in LRR-RP-dependent PTI, we screened an Arabidopsis RLCK-VII transfer DNA mutant library 10 for ethylene production elicited by fungal pg13(At) 11 , oomycete nlp20 and bacterial eMax (which are recognized by RLP42, RLP23 and RLP1, respectively) 3 (Extended Data Fig. 1a). A pbl31 mutant was defective in response to these elicitors compared with wild-type plants (Columbia-0 (Col-0)) (Extended Data Fig. 1a). PBL31 belongs to RLCK-VII subfamily 7, together ...

An atypical NLR protein modulates the NRC immune receptor network

“…NLRs perceive pathogen secreted proteins known as effectors and induce robust immune responses that generally include hypersensitive cell death (Jones et al, 2016;Kourelis and van der Hoorn, 2018;Saur et al, 2021). NLR-mediated immunity (also known as effector-triggered immunity) can be effective in restricting pathogen infection at invasion sites, and NLRs have also been recently shown to be involved in PRR-mediated signalling (Ngou et al, 2021a;Pruitt et al, 2021;Tian et al, 2021;Kourelis et al, 2021b). However, NLR-mediated immunity comes at a cost for plants.…”

Plant immunity: Rice XA21-mediated resistance to bacterial infection

“…The PTI/ETI distinction as originally proposed has blurred with the discovery and characterization of more receptor/ligand pairs and their downstream partners, which have revealed the overlap between resistance mechanisms ( 20 , 52 , 93 ). Similarly, as more microbial factors are identified that do not neatly fit into the PAMP vs. effector dichotomy, such classifications may lose relevance ( 91 , 94 – 97 ).…”

“…SOBIR1 interacts with RLP23 to facilitate immune response to Pst ( 142 ). The RLP23/SOBIR1 complex, which also requires BAK1 coreceptor for function, is particularly interesting because the output requires proteins that were previously shown to be essential to immunity mediated by the NBS-LRR intracellular class of receptors ( 94 ). In addition to Arabidopsis RLP23, SOBIR is essential for the function of other RLPs, such as Cf-4 in tomato, indicating its broad involvement in RLP-mediated immunity as a coreceptor ( 94 , 141 ).…”

A Glimpse of Programmed Cell Death Among Bacteria, Animals, and Plants

“…PTI can enhance resistance from PTI. The PTI and ETI comprising the two-tiered plant immune system that monitors threats from pathogens are not separable and collaboratively contribute to the reciprocal enhancement of plant immunity ( Ngou et al, 2021 ; Pruitt et al, 2021 ; Yuan et al, 2021 ; Tian et al, 2021 ). HR as one canonical type of PCD in plants is beneficial to the host likely by eliminating the intracellular niche for proliferation of certain pathogens.…”

“…Reprogramming of immune genes enforces resistance. The ADR1-EDS1-PAD4 module can be polymerized with the complex formed by LRR-RP-SOBIR1 and PBL31 of the RLCK family to form a supramolecular complex, which not only binds the inner leaflet of the plasma membrane to mediate the response of PTI but ADR1 is contributive to TNL-directed resistance signaling involved in reprogrammed transcription of pathogenesis-responsive genes ( Pruitt et al, 2021 ) ( Figure 3C ).…”