A molecular roadmap to the plant immune system

Abstract

Plant diseases caused by pathogens and pests are a constant threat to global food security. Direct crop losses and the measures used to control disease (e.g. application of pesticides) have significant agricultural, economic, and societal impacts. Therefore, it is essential that we understand the molecular mechanisms of the plant immune system, a system that allows plants to resist attack from a wide variety of organisms ranging from viruses to insects. Here, we provide a roadmap to plant immunity, with a focus on cell-surface and intracellular immune receptors. We describe how these receptors perceive signatures of pathogens and pests and initiate immune pathways. We merge existing concepts with new insights gained from recent breakthroughs on the structure and function of plant immune receptors, which have generated a shift in our understanding of cell-surface and intracellular immunity and the interplay between the two. Finally, we use our current understanding of plant immunity as context to discuss the potential of engineering the plant immune system with the aim of bolstering plant defenses against disease.

Keywords: Nod-like receptor (NLR); cell surface receptor; cell-surface immunity; cellular immune response; effectors; intracellular immunity; nucleotide-binding leucine-rich repeat receptors (NLRs); plant biochemistry; plant defense; plant immunity; receptor-like kinases (RLKs); receptor-like proteins (RLPs); resistance engineering.

Figure 1.

Plant immunity at a glance. Left, plants are the target of a variety of pathogens and pests that cause disease, via both their above-ground and underground structures. Right, pathogens/pests shed MAMPs or generate DAMPs that can be received by receptors to initiate cell-surface immunity. Pathogens/pests can deliver effectors to the outside (not shown here for simplicity) or inside of cells, where they can act on host systems to their benefit, including the suppression of signaling pathways downstream of cell-surface receptors. Effectors or their activities can be sensed by intracellular immune receptors (NLRs) to initiate intracellular immunity.

Figure 2.

Diversity of cell-surface immune receptors. A schematic representation depicts the domain architecture of different classes of plant RLKs/RLPs. Surface representations are shown for those ECDs for which crystal structures are available. LRR, crystal structure of the ECD of Arabidopsis RLK FLS2, PDB entry 4MNA (green); LysM, crystal structure of the ECD of Arabidopsis RLK–CERK1, PDB entry 4EBY (purple).

Figure 3.

A mechanistic view of flg22 sensing by FLS2. flg22 (light green) stabilizes the heterodimerization of FLS2 (dark green, PDB entries 4NMA and 4NM8) with BAK1 (purple, PDB entries 3ULZ and 4NM8) (82, 85, 86). Ligand perception leads to activation and phosphorylation of BIK1 (orange, PDB entry 5TOS) by BAK1 (87, 88). Following phosphorylation, BIK1 is monoubiquitinated (Ub) by the E3 ligases RHA3A/B. Monoubiquitinated BIK1 is then released from the FLS2–BAK1 complex and initiates ROS production and Ca²⁺ signaling through phosphorylation of plasma membrane–localized NADPH oxidases and cyclic nucleotide–gated channels (89). The bidirectional arrow indicates that both BIK1 and BAK1 can trans-phosphorylate each other.

Figure 4.

NLRs perceive effectors via distinct mechanisms and induce immune responses through different mechanisms. A, effector (purple) perception induces activation of the NLR (orange) via direct binding. NLRs can indirectly perceive and respond to effectors by monitoring modifications of a physiologically relevant host target (Guardee, gray) or a molecular mimic that likely resulted via gene duplication and is now only involved in immune signaling (Decoy, blue). NLRs can directly perceive and respond to effectors via NLR integrated domains (blue), which likely have their evolutionary origin in ancestral host targets of effectors. B, NLR singletons are able to initiate immune responses upon effector perception. Several sensor NLRs require downstream helper NLRs (green) to transduce effector perception into immune responses. NLRs can function in pairs or as part of interconnected networks.

Figure 5.

Incorporation of host targets in NLRs leads to the evolution of NLR with integrated domains. NLRs (orange) can sense changes in host proteins (gray) that are targeted by pathogen effector molecules (purple) and initiate defense signaling. Over time, some of these host proteins can be found integrated into the NLR core structure (blue), acting as the effector recognition domains for the NLR. Binding of an effector to the integrated domain of an NLR leads to initiation of defense responses.

Figure 6.

The activation of the ZAR1 immune receptor. ZAR1 (orange) is an Arabidopsis CC-NLR that forms complexes with pseudokinases, including ZED1 and RKS1 (green), to perceive effector activity (208). The ZAR1:RKS1 receptor complex guards the receptor-like cytoplasmic decoy kinase PBL2. Following uridylylation of PBL2 by the Xanthomonas campestris effector protein AvrAC, PBL2^UMP (purple) binds to RKS1, activating ZAR1. Activated ZAR1 is then able to oligomerize into a pentameric wheel with the CC domains each contributing their H1 helix (yellow) to form a funnel-like structure.

Figure 7.

Alternative strategies for immune receptor engineering. A, plant immune receptors (orange/gray) bind natural variants of effector and ligands (purple/cyan/yellow) with different binding affinities (schematically depicted by the height of the colored bars). Only some binding events are of sufficient level to reach an activation threshold (represented by the dashed line), triggering immune responses. B, mutations in the receptor (gray to blue) can extend pathogen recognition by gaining or increasing binding to effectors and ligands, leading to immune responses to pathogens previously undetected. C, mutations in the immune receptors (orange to green) can lower the activation threshold, allowing for increased intensity of immune signaling. D, the combination of both mutations (green/blue receptor) that enhance recognition and immune responses can lead to wider and increased immune responses to effectors and ligands.