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Cell Death in Plant Immunity - PubMed

  • ️Wed Jan 01 2020

Review

Cell Death in Plant Immunity

Eugenia Pitsili et al. Cold Spring Harb Perspect Biol. 2020.

Abstract

Pathogen recognition by the plant immune system leads to defense responses that are often accompanied by a form of regulated cell death known as the hypersensitive response (HR). HR shares some features with regulated necrosis observed in animals. Genetically, HR can be uncoupled from local defense responses at the site of infection and its role in immunity may be to activate systemic responses in distal parts of the organism. Recent advances in the field reveal conserved cell death-specific signaling modules that are assembled by immune receptors in response to pathogen-derived effectors. The structural elucidation of the plant resistosome-an inflammasome-like structure that may attach to the plasma membrane on activation-opens the possibility that HR cell death is mediated by the formation of pores at the plasma membrane. Necrotrophic pathogens that feed on dead tissue have evolved strategies to trigger the HR cell death pathway as a survival strategy. Ectopic activation of immunomodulators during autoimmune reactions can also promote HR cell death. In this perspective, we discuss the role and regulation of HR in these different contexts.

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Figures

Figure 1.
Figure 1.

Plant NLRs (nucleotide-binding domain leucine-rich repeat (LRR)-containing gene family). (A) Schematic representation of a plant NLR protein. The amino-terminal region usually contains a Toll/interleukin-1 receptor (TIR) homology or a coiled-coil (CC) domain. The central region is composed of a nucleotide-binding APAF-1, R proteins, and CED-4 (NB-ARC) domain. The carboxy-terminal region contains an LRR domain. (B) NLR activation. In the inactive, closed state, ADP is bound to the NB-ARC domain. Direct or indirect effector recognition, results in ADP release and ATP binding. This results in a conformational change that renders an open, active NLR.

Figure 2.
Figure 2.

Pathways leading to hypersensitive response (HR) cell death in plant immunity. (1) HR can be triggered on recognition of a biotrophic or hemibiotrophic pathogen via direct or indirect effector recognition by NLR (nucleotide-binding domain leucine-rich repeat-containing gene family) immune receptors, often operating in pairs (sensor NLR + helper NLR). (2) Cell death–specific modules have been identified, which translate the signal generated by effector perception via Toll/interleukin-1 receptor domain NLR (TIR-NLR) activation, into HR cell death. (3) Pattern-recognition receptors (PRRs) signaling at the plasma membrane may be monitored by NLRs, with PRR signaling disturbance leading to HR cell death. (4) HR cell death can be genetically uncoupled from local defense responses, but may have a role in activating systemic resistance responses. (5) HR can occur as a result of autoimmune reactions, owing to the ectopic activation of NLRs or other defense signaling modulators or an NLR mismatch. (6) Necrotrophic fungi can cause disease by hijacking the host HR cell death. A common strategy is activation of NLR receptors by toxins secreted by the fungi into the plant cytoplasm.

Figure 3.
Figure 3.

Mechanism of resistosome activation. (1) In its resting state, the NLR HOPZ-ACTIVATED RESISTANCE 1 (ZAR1) is bound to ADP and the RLCK RESISTANCE-RELATED KINASE 1 (RKS1). (2) Xanthomonas campestris secretes the effector AvrAC into the host plant cells, which uridylates the RLCK PBS1-LIKE PROTEIN 2 (PBL2). (3) Uridylated PBL2 binds to RKS1, causing conformational changes to the ZAR1–RKS1 dimer that release ADP and prime the complex for activation. (4) Subsequent ATP binding results in formation of the resistosome via pentamerization of the ZAR1–RKS1–PBL2 complex. (5) Conformational changes expose a funnel-like structure essential for accumulation of the complex in the plasma membrane, bacterial resistance, and (6) cell death, which has been hypothesized to be mediated by pore formation at the plasma membrane on insertion of the resistosome.

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