Effector-Triggered Immunity in Plants
Plants rely on multiple immune systems to protect themselves from pathogens. When pattern-triggered immunity (PTI)—the first layer of the immune response—is no longer effective as a result of pathogenic effectors, effector-triggered immunity (ETI) often provides resistance. In ETI, host plants directly or indirectly perceive pathogen effectors via resistance proteins and launch a more robust and rapid defense response. Resistance proteins are typically found in the form of nucleotide-binding and leucine-rich-repeat-containing receptors (NLRs). Upon effector recognition, an NLR undergoes structural change and associates with other NLRs. The dimerization or oligomerization of NLRs signals to downstream components, activates “helper” NLRs, and culminates in the ETI response. Originally, PTI was thought to contribute little to ETI. However, most recent studies revealed crosstalk and cooperation between ETI and PTI.
2. The Evolution of Pathogen Perception by NLRs
3. NLR Activation and Signaling Events Following Pathogen Recognition
3.1. Multi-Domain NLRs Act as Molecular Switches
3.2. Homo/Hetero-Complex Formation Is Necessary for NLR Signaling
Previous studies reported that disruption of the Mildew A 10 (MLA10) CC dimerization abolished the activation of immunity , suggesting that CNLs require dimerization of the CC domain for signal transduction. Moreover, pentameric oligomerization of the CNL Hrp-dependent outer protein (Hop) Z-Activated Resistance 1, termed the “HopZ-Activated Resistance 1 resistosome”, is important for the formation of putative membrane pores and the immune response . Similarly, several well-studied plant NLRs containing TIR domains, such as RECOGNITION OF PERONOSPORA PARASITICA 1 (RPP1), the flax resistance protein L6, RRS1, and RPS4, were found to require oligomerization by two distinct interfaces, for both self-association and defense signaling . Similar to the case of MLA10, disrupting the homo-dimerization of L6 TIRs interferes with downstream signaling (Figure 2B). To effectively recognize the effector Xanthomonas outer protein Q (XopQ), the TNL Recognition of XopQ 1 resistosome requires tetramerization . In addition, two asymmetric TIR homodimers that form an RPP1 tetrameric resistosome activate downstream signaling, in response to effector Arabidopsis thaliana Recognized 1(Figure 2B) .
Hetero-associations in addition to homo-dimerization were proven to be an indispensable aspect in NLR-mediated signaling. Indeed, genetically-linked paired NLRs were characterized as functioning together in conferring pathogen resistance . RGA4/RGA5 is one of the functionally paired CNLs for Magnaporthe oryzae AVR-Pia/AVR-Pik-mediated resistance . In addition, genetically-linked, paired TNLs, such as RPP2A/RPP2B, were found to provide resistance against Hpa race Cala 2 , along with previously discussed RRS1/RPS4 recognize AvrRps4 and PopP2 . In the paired cases listed above, one NLR, the “sensor NLR”, usually contains an evolutionarily incorporated integrated domain, and acts as an effector receptor, while the second NLR, the “executor NLR”, induces downstream signaling .
3.3. Intramolecular Regulation of Guardee/Decoy Contributes to NLR-Mediated Resistance
It is now clear that R proteins can guard plant functions by monitoring different post-translational modifications of effector targets (guardee/decoy), and that different modifications can compete with or support each other. RIN4 was proposed to act as a phosphoswitch to detect the effector AvrRpm1. Targeting of RIN4 by AvrRpm1 causes the phosphorylation of threonine 166 within its C-terminal nitrate-induced domain; which leads to RPM1 activation and resistance . A recent study revealed that the ADP-ribosylation of RIN4 at aspartate 153 by AvrRpm1, leads to threonine 166 phosphorylation and promotes RPM1 activation . The addition of ADP-ribose supports the complete phosphorylation of threonine 166 in RIN4 . Taken together, these reports indicate that several additive modifications can occur in a single guardee protein.
On the other hand, a post-translational modification of one effector target can antagonize another. The newest report of RRS1/RPS4-mediated immunity revealed that phosphorylation regulates the activation of paired RRS1/RPS4 . In the absence of effector AvrRps4 or PopP2, phosphorylation at threonine 1214 in the integrated decoy WRKY domain keeps RRS1 from the resistant ecotype Wassilewskija, in a resting state. Dephosphorylation at that residue leads to the autoactivation of RRS1. Interestingly, PopP2 induces O-acetylation in the WRKY domain of RRS1, which competes with its phosphorylation and results in the dephosphorylated activated RRS1-mediated resistance to Ralstonia Solanacearum . Other phosphorylation sites at the C terminus of RRS1 are required for PopP2 recognition, which enhances the interaction of the TIR domain with the WRKY domain. This study also proved that wild-type Columbia RRS1 lacks the C-terminal 83 amino acids that include the target phosphorylation sites, fails to recognize PopP2, and is thus susceptible to Ralstonia Solanacearum.
However, RRS1-mediated resistance to the Pseudomonas syringae effector AvrRps4 is determined by the association of the RRS1 C-terminus with its TIR, not by its phosphorylation status . The C terminus and TIR of RRS1 interact with each other only in the presence of AvrRps4 . During recognition of AvrRps4 or PopP2, the interaction of the RRS1 TIR domain with its C terminus is enhanced. This enhanced interaction releases the RPS4 TIR from the inhibition by the RRS1 TIR. Thus, the RPS4 TIR is activated, resulting in resistance to Pseudomonas syringae. The regulation of guardee/decoy monitoring is likely much more complex than is presently known.
3.4. News-Breaking: Enzyme Activity of Plant TIR in ETI Signaling
In animal immunity, an important function of Toll-like receptors is specifically recognizing their cognate pathogen-associated molecular patterns or synthetic compounds. Most animal Toll-like receptors contain two domains, one of which—the LRR domain—is necessary for PAMP recognition, while the other—the TIR domain—functions in signaling scaffolds. Some studies of animal-TIR domain crystallization showed that animal TIR associates during PAMP recognition. Animal TIR oligomerization is required for immune signaling, leading to the inflammatory cytokine response . Unlike most Toll-like receptors, Sterile Alpha and TIR Motif Containing 1 (SARM1) was shown to have a surprisingly novel function . Specifically, the nicotinamide adenine dinucleotide (NAD) hydrolase activity of its TIR domain contributes to axon degradation. This unique function raised the hypothesis that SARM1 probably arose from other domains in the animal system, through an evolutionary transfer event .
In plants, after NLR activation, the subsequent signal transduction cascade leading to the hypersensitive response and expression of plant immunity is at present unresolved. Although the signaling pathway of CNLs remains unclear, a piece of TNL downstream signaling was discovered . As TIR domains are found in both plant intracellular TNLs and the animal cell surface Toll-like receptors, researchers compared the characteristics of plant TIR and animal TIR. Wan et al. and Horsefield et al. demonstrated that the TIR domains of plant TNLs are structurally similar to the TIR domain of mammalian SARM1 and that their enzymatic activity could degrade oxidized nicotinamide adenine dinucleotide (NAD+) (Figure 2C) . Cell death activation and NAD+ catalytic activity of plant TIRs are self-association interface-dependent, placing the TIR enzyme activity downstream of TIR oligomerization. A conserved glutamic acid was found in plant TIR NAD+-cleaving enzymes and the human SARM1 NADase . Although the putative catalytic glutamic acid does not affect the TIR association, it is the key residue for TIR-NADase activation. The accumulation of enzymatic products, such as variant-cyclic ADP-Ribose (v-cADPR), ADP-Ribose, and nicotinamide, which are necessary for immune signaling, are proposed to be downstream of TIR-enzyme activation. The NADase activity of the plant TIR domain is solely required for plant immunity, since the fusion of plant TIR (not animal or bacterial TIR) to the mammalian NLR Family CARD Domain Containing 4 activates immune signaling in plants . Interestingly, in both enhanced disease susceptibility 1 (eds1) and n requirement gene 1 (nrg1) mutants, the activation of RBA1 accumulates v-cADPR but fails to induce a cell-death response , indicating that the accumulation of enzymatic products happens upstream of EDS1-NRG1. However, from catalytic product accumulation to EDS1-NRG1 downstream signaling, an undefined gap remains.
4. Helper NLR Cooperation beyond Genetically Linked Pairs
5. PTI/ETI Unity Produces Full Plant Immunity
The entry is from 10.3390/ijms22094709
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