Pattern-recognition receptors in plant innate immunity

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Perception of pathogen-associated molecular patterns (PAMPs) constitutes the first layer of plant innate immunity and is referred to as PAMP-triggered immunity (PTI). For a long time, part of the plant community was sceptical about the importance of PAMP perception in plants. Genetic and biochemical studies have recently identified pattern-recognition receptors (PRRs) involved in the perception of bacteria, fungi and oomycetes. Interestingly, some of the structural domains present in PRRs are similar in plants and animals, suggesting convergent evolution. Lack of PAMP perception leads to enhanced disease susceptibility, demonstrating the importance of PAMP perception for immunity against pathogens in vivo. Recently, proteins with known roles in development have been shown to control immediate PRR-signalling, revealing unexpected complexity in plant signalling. Although many PAMPs recognised by plants have been described and more are likely to be discovered, the number of PRRs known currently is limited. The study of PTI is still in its infancy but constitutes a highly active and competitive field of research. New PRRs and regulators are likely to be soon identified.

Introduction

Plants lack the adaptive immunity mechanisms of jawed vertebrates, so rely on innate immune responses for defense. As sessile organisms they are subject to changing environmental conditions including constant pathogen attack. However, would-be pathogens must first penetrate barriers such as wax layers or rigid cell walls. A pathogen that overcomes these obstacles is subject to molecular recognition by plant cells. Plants lack circulating cells specialised in microbe recognition such as macrophages. Instead, each cell is able to recognise and respond to pathogens autonomously. In addition, systemic signalling can be triggered in response to microbial stimuli that prepare naïve tissue for imminent attack. Overall, plant innate immunity is very efficient and most plants are resistant to most microbes. Part of this success is because of an amazing spectrum of recognition specificities encoded by all cells.

Plants initially sense microbes via perception of pathogen-associated molecular patterns (PAMPs) by pattern-recognition receptors (PRRs) located on the cell surface. PAMPs are conserved, indispensable molecules that are characteristic of a whole class of microbes and therefore are difficult to mutate or delete. They are also referred to as microbe-associated molecular patterns (MAMPs), as they are not restricted to pathogenic microbes. This first level of recognition is referred to as PAMP-triggered immunity (PTI). Intracellular responses associated with PTI include rapid ion fluxes across the plasma membrane, MAP kinase activation, production of reactive-oxygen species, rapid changes in gene expression and cell wall reinforcement. Successful pathogens have evolved strategies to infect host plants, either by evading recognition or by suppressing the subsequent signalling steps. In many cases, suppression of PTI involves secretion of virulence effectors by the pathogens. In a dynamic co-evolution between plants and pathogens, some plants have evolved resistance proteins (R proteins) to recognise these effectors directly or indirectly. This so-called effector-triggered immunity (ETI) is often accompanied by local cell death known as the hypersensitive response (HR). In turn, pathogens have evolved effectors capable of suppressing ETI, and so the arms-race between host and pathogens unfolds.

In this model, PTI is the first facet of active plant defense and can therefore be considered as the primary driving force of plant–microbe interactions. Given the complexity of plant innate immunity as a whole, I will focus here on recent developments in PAMP perception by plants. For aspects related to PTI signalling, PTI suppression by effectors and ETI, readers are directed to excellent recent reviews [1••, 2••, 3, 4, 5, 6, 7].

PAMP perception in mammals mostly depends on transmembrane proteins, such as Toll-like receptors (TLRs), ‘Triggering Receptors Expressed on Myeloid cells’ (TREMs), Siglec5 and C-type lectin receptors (CLRs) [8]. However, the important role of cytoplasmic Nod (nucleotide-binding oligomerisation domain)-like receptors (NLRs) as mammalian PRRs has also been recently demonstrated [9]. Although plant ETI mostly involves NLR-like R proteins, no cytoplasmic plant PRRs have yet been identified and known plant PRRs correspond so far only to transmembrane or secreted proteins. Plants do not possess obvious orthologues of mammalian transmembrane PRRs. However, some of the domains potentially involved in PAMP recognition and signalling are conserved between plants and animals, suggesting that the different kingdoms have recruited similar mechanisms to perceive microbes [10, 11].

Section snippets

Flagellin recognition: an ever-expanding model

The best-characterised PAMP in plants is the flagellin protein that constitutes the main building block of eubacterial flagella. Most plant species recognise a highly conserved 22-amino-acid epitope, flg22, present in the flagellin N-terminus [12]. The PRR responsible for flagellin recognition in the plant model Arabidopsis thaliana is the leucine-rich repeat receptor-like kinase (LRR-RLK) FLAGELLIN-SENSING 2 (FLS2) [13••]. LRR-RLKs are single-pass transmembrane proteins composed of an LRR

EF-Tu: an unexpected PAMP?

Elongation factor Tu (EF-Tu) is the most abundant bacterial protein and is recognised as a PAMP in Arabidopsis and other members of the family Brassicaceae [26]. A highly conserved N-acetylated 18 amino acid peptide, elf18, is sufficient to trigger those responses induced by full-length EF-Tu. Peptides derived from plant mitochondrial or plastid EF-Tu are inactive as PAMPs, revealing that this perception is specific to the infectious non-self.

The PRR for EF-Tu is the LRR-RLK EF-TU RECEPTOR

LRR-receptor kinases do not explain everything

FLS2 and EFR are so far the only known PRRs in Arabidopsis, but also the only known PRRs that recognise bacterial PAMPs in plants. Other examples of plant PRRs are very scarce (Figure 1).

In legumes, a soluble β-glucan-binding protein (GBP) is the specific binding site for the 1,6-β-linked and 1,3-β-branched heptaglucoside (HG) present in the cell wall of the oomycete Phytophtora sojae. Interestingly, GBP also exhibits an intrinsic endo-1,3-β-glucanase activity [32]. Therefore, GBP can both

PRRs do not signal alone

The best-studied LRR-RLK in plants is BRASSINOSTEROID INSENSITIVE 1 (BRI1), the receptor for the brassinosteroid hormones (BRs) which control many aspects of growth and development. Although BRI1 contains the BR-binding site, it requires another LRR-RLK named BRI1-ASSOCIATED KINASE 1 (BAK1) for proper signalling [39]. Unexpectedly, BAK1 was identified as a positive regulator of both FLS2 and EFR [40••, 41••]. BAK1 is dispensable for flg22 binding, but interacts with FLS2 in a ligand-dependent

Conclusions and perspectives

We clearly need to identify new PAMPs and their corresponding PRRs to reveal the span of PAMP perception in a given plant species. Classical bacterial PAMPs recognised in animals, such as lipopolysaccharides [50] and peptidoglycans [51] are also recognised by plants, but their receptors are still unknown. Plants can also recognise microbial toxins to activate defense [52]. Plants are also able to sense the infectious-self, that is, host molecules that are normally not available for

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

I apologise to colleagues who could not be cited due to strict space limitations. The research in my lab is supported by the Gatsby Charitable Foundation. I would like to thank John Rathjen and Volker Lipka for comments on the manuscript and stimulating discussions.

References (57)

  • J.D. Jones et al.

    The plant immune system

    Nature

    (2006)
  • R.B. Abramovitch et al.

    Bacterial elicitation and evasion of plant innate immunity

    Nat Rev Mol Cell Biol

    (2006)
  • A.F. Bent et al.

    Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions

    Annu Rev Phytopathol

    (2007)
  • D. Altenbach et al.

    Pattern recognition receptors: from the cell surface to intracellular dynamics

    Mol Plant Microbe Interact

    (2007)
  • P. Bittel et al.

    Microbe-associated molecular patterns (MAMPs) probe plant immunity

    Curr Opin Plant Biol

    (2007)
  • T.A. Kufer et al.

    Sensing of bacteria: NOD a lonely job

    Curr Opin Microbiol

    (2007)
  • C. Zipfel et al.

    Plants and animals: a different taste for microbes?

    Curr Opin Plant Biol

    (2005)
  • D. Chinchilla et al.

    The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception

    Plant Cell

    (2006)
  • S.H. Shiu et al.

    Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases

    Proc Natl Acad Sci U S A

    (2001)
  • S. Robatzek et al.

    Molecular identification and characterization of the tomato flagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities

    Plant Mol Biol

    (2007)
  • D.R. Hann et al.

    Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana

    Plant J

    (2007)
  • C. Zipfel et al.

    Bacterial disease resistance in Arabidopsis through flagellin perception

    Nature

    (2004)
  • M. de Torres et al.

    Pseudomonas syringae effector AvrPtoB suppresses basal defence in Arabidopsis

    Plant J

    (2006)
  • X. Li et al.

    Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors

    Proc Natl Acad Sci U S A

    (2005)
  • W. Sun et al.

    Within-species flagellin polymorphism in Xanthomonas campestris pv. campestris and its impact on elicitation of Arabidopsis FLAGELLIN SENSING2-dependent defenses

    Plant Cell

    (2006)
  • C. Pfund et al.

    Flagellin is not a major defense elicitor in Ralstonia solanacearum cells or extracts applied to Arabidopsis thaliana

    Mol Plant Microbe Interact

    (2004)
  • R. Takai et al.

    A new method of defense response analysis using a transient expression system in rice protoplasts

    Biosci Biotechnol Biochem

    (2007)
  • S. Fujiwara et al.

    Rice cDNA microarray-based gene expression profiling of the response to flagellin perception in cultured rice cells

    Mol Plant Microbe Interact

    (2004)
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