Perception of structurally distinct effectors by the integrated WRKY domain of a plant immune receptor

Abstract

Plants use intracellular nucleotide-binding domain (NBD) and leucine-rich repeat (LRR)–containing immune receptors (NLRs) to detect pathogen-derived effector proteins. The Arabidopsis NLR pair RRS1-R/RPS4 confers disease resistance to different bacterial pathogens by perceiving the structurally distinct effectors AvrRps4 from Pseudomonas syringae pv. pisi and PopP2 from Ralstonia solanacearum via an integrated WRKY domain in RRS1-R. How the WRKY domain of RRS1 (RRS1WRKY) perceives distinct classes of effector to initiate an immune response is unknown. Here, we report the crystal structure of the in planta processed C-terminal domain of AvrRps4 (AvrRps4C) in complex with RRS1WRKY. Perception of AvrRps4C by RRS1WRKY is mediated by the β2-β3 segment of RRS1WRKY that binds an electronegative patch on the surface of AvrRps4C. Structure-based mutations that disrupt AvrRps4C–RRS1WRKY interactions in vitro compromise RRS1/RPS4-dependent immune responses. We also show that AvrRps4C can associate with the WRKY domain of the related but distinct RRS1B/RPS4B NLR pair, and the DNA-binding domain of AtWRKY41, with similar binding affinities and how effector binding interferes with WRKY–W-box DNA interactions. This work demonstrates how integrated domains in plant NLRs can directly bind structurally distinct effectors to initiate immunity.

A Comprehensive Study of the WRKY Transcription Factor Family in Strawberry

“…Among the R protein-WRKY subclass, FaWRKY55D was the only one differentially expressed at early stages of the infection. This is particularly interesting as it could be hypothesized that FaWRKY55D could participate in the activation of the early immune response in strawberry similarly to the RRS1-R/RSP4 pair system (via an integrated WRKY domain in RRS1-R) recently described in Arabidopsis [100,101]. Therefore, it should be included in the repertory of putative candidate strawberry WRKY defense-responsive genes for further study.…”

“…Most of them showed relatively high transcript abundances in leaves, roots and fruit tissues also, suggesting that changes in their gene expression, if any, are either not needed to play positive roles against pathogens or these changes are pathogen-specific deployed or involved in other plant processes. Nevertheless, their roles in the strawberry physiology remain unknown, as the vast majority of other R protein-WRKY in several species [100,101]. From the currently available data, a selection of putative candidate FaWRKY genes for further research is shown in Table S19.…”

Effector target-guided engineering of an integrated domain expands the disease resistance profile of a rice NLR immune receptor

“…This is exemplified by the TIR-NLR pair RRS1 and RPS4, which mediate recognition of the structurally distinct effectors PopP2 from Ralstonia solanacearum and AvrRps4 from Pseudomonas syringae pv. pisi (10, 11, 24–27). Furthermore, the potential to replace naturally occurring integrated domains with nanobodies of defined specificity to confer disease resistance has recently been demonstrated (28).…”

“…In addition, some NLRs contain non-canonical domains which are integrated into the protein architecture either at the N-or C-termini or between canonical domains (3)(4)(5)(6). These integrated domains (IDs) resemble effector virulence targets and either directly bind or are modified by effector proteins to activate NLR-mediated immune signalling (4,(7)(8)(9)(10)(11).…”

“…This is exemplified by the TIR-NLR pair RRS1 and RPS4, which mediate recognition of the structurally distinct effectors PopP2 from Ralstonia solanacearum and AvrRps4 from Pseudomonas syringae pv. pisi (10,11,(24)(25)(26)(27).…”