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Regulation of pattern recognition receptor signalling in plants

Key Points

  • Plants rely on a cell-autonomous innate immune system to detect the presence of microorganisms and activate immune responses that deter infection. Recognition of conserved microbial features occurs essentially at the cell surface by means of transmembrane pattern recognition receptors (PRRs).

  • PRRs are part of multimeric protein complexes at the plasma membrane, differentially recruiting cytoplasmic kinases that connect PRR complexes to downstream signalling components.

  • Ligand binding initiates a series of phosphorylation events within PRR complexes that activates cellular immune signalling, which includes bursts of intracellular reactive oxygen species and calcium, activation of cytoplasmic kinase cascades, and transcriptional reprogramming.

  • As in mammals, excessive activation of plant immune responses can have detrimental consequences. Thus, a complex negative regulatory system controls different immune components to maintain cellular homeostasis.

  • Bacterial pathogens are able to subvert the plant immune system by secreting molecules, such as effectors, that often mimic the mode-of-action of host negative regulators of immune signalling.

Abstract

Recognition of pathogen-derived molecules by pattern recognition receptors (PRRs) is a common feature of both animal and plant innate immune systems. In plants, PRR signalling is initiated at the cell surface by kinase complexes, resulting in the activation of immune responses that ward off microorganisms. However, the activation and amplitude of innate immune responses must be tightly controlled. In this Review, we summarize our knowledge of the early signalling events that follow PRR activation and describe the mechanisms that fine-tune immune signalling to maintain immune homeostasis. We also illustrate the mechanisms used by pathogens to inhibit innate immune signalling and discuss how the innate ability of plant cells to monitor the integrity of key immune components can lead to autoimmune phenotypes following genetic or pathogen-induced perturbations of these components.

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Figure 1: Recruitment of regulatory receptor kinases and RLCKs by PRRs in Arabidopsis and rice.
Figure 2: Early branching of PRR-triggered immunity signalling.
Figure 3: Negative regulation of PTI signalling by a multi-layered system.
Figure 4: Negative regulation at the PRR complex level.

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Acknowledgements

The authors would like to thank all members of the Zipfel laboratory for fruitful discussions, especially N. Holton and M. Stegmann, as well as S. Ben Khaled, for critically reading the manuscript before submission. D.C. was supported by a Ph.D. scholarship (reference SFRH/BD/79088/2011) from Fundação para a Ciência e a Tecnologia (FCT). Research in the Zipfel laboratory is funded by the Gatsby Charitable Foundation, the European Research Council (ERC), the UK Biotechnology and Biological Sciences Research Council (BBSRC), and the Two Blades Foundation.

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Correspondence to Cyril Zipfel.

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Glossary

Receptor kinases

Plasma membrane-localized proteins characterized by a ligand-binding ectodomain, a single-pass transmembrane domain and an intracellular signalling kinase domain. Different types of ectodomain determine their ligand-binding specificity. Receptor kinases may act as the main receptor or as co-receptor or regulatory protein.

Receptor-like proteins

(RLPs). Surface-localized proteins similar to receptor kinases but lacking an obvious intracellular signalling domain. RLPs typically require regulatory receptor kinases to initiate signalling.

Plasmodesmata

Intercellular cytoplasmic bridges equivalent to gap junctions that allow communication and transport of molecules between plant cells. During pathogen infection, plasmodesmata can be sealed by deposition of callose layers to isolate infected areas.

Stomata

Natural openings in the leaf epidermis formed by two guard cells that enable gaseous exchange and are often used by pathogenic microorganisms to enter the leaf.

EF-hand motifs

Helix–loop–helix protein motifs involved in Ca2+ binding.

Callose

A (1,3)-β-glucan polymer present in the plant cell wall. Deposition of callose occurs upon pathogen recognition, forming cell wall thickenings.

Exocyst complex

An octameric complex involved in the tethering of exocytic vesicles to their site of fusion in the plasma membrane.

Phytoalexin

Antimicrobial compounds produced by plants during pathogen infection.

Camalexin

Typical Arabidopsis phytoalexin produced in response to pathogen infection; it is also known as 3-thiazol-2′-yl-indole.

VQ proteins

(VPQs). A class of plant-specific proteins with a conserved FxxφVQxφTG amino acid motif (VQ motif; x representing any amino acid and φ representing hydrophobic residues).

Salicylic acid

A phenolic plant hormone with a major role in plant defence against biotrophic pathogens. Its acetylated form (acetylsalicylic acid) is commonly known as aspirin, a widely prescribed anti-inflammatory drug.

Jasmonic acid

The best-studied member of the jasmonates family of oxylipin plant hormones. Jasmonates are typically synthesized during responses against necrotrophic pathogens and herbivores.

Auxin

A class of plant growth hormone, existing mostly as free or conjugated forms of indole-acetic acid (IAA), which is a tryptophan derivative. Auxin has a pivotal role in various key developmental processes, such as cell expansion and division, root and stem elongation, and flowering.

Cytokinins

Plant growth hormones, derived from adenine, that are known to promote cell division and differentiation.

Brassinosteroids

A class of polyhydroxysteroid plant hormone required for several developmental and physiological processes. Brassinosteroids are perceived at the cell surface by the leucine-rich repeat (LRR)- receptor kinase BRI1, which recruits the co-receptor BAK1 to initiate brassinosteroid-mediated signalling.

Gibberellin

Diterpene-type plant growth hormones involved in several developmental processes, such as seed germination, stem elongation and fruit maturation.

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Couto, D., Zipfel, C. Regulation of pattern recognition receptor signalling in plants. Nat Rev Immunol 16, 537–552 (2016). https://doi.org/10.1038/nri.2016.77

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