Trends in Plant Science
Volume 14, Issue 10, October 2009, Pages 521-529
Journal home page for Trends in Plant Science

Opinion
NB-LRRs work a “bait and switch” on pathogens

https://doi.org/10.1016/j.tplants.2009.08.001Get rights and content

Plant genomes encode large numbers of highly variable nucleotide binding leucine-rich repeat (NB-LRR) disease resistance proteins. These proteins have been studied extensively to understand their evolution and the molecular basis of their function. Multiple studies indicate that the C-terminal LRR domain plays a pivotal role in defining pathogen recognition specificity. However, a growing body of evidence suggests that the N-termini of NB-LRR proteins also function in pathogen recognition. To formulate a framework that can explain the underlying principles governing NB-LRR function while accommodating findings from different experimental systems, we present a “bait and switch” model. This model proposes a two-step recognition process involving interactions with both cellular cofactors (bait) and the LRR domain, which in turn activates the molecular switch leading to disease resistance.

Section snippets

NBLing away at pathogens

Plants employ a network of intertwined mechanisms to counter infection by pathogens and parasites. One such line of defense is based on dominant disease resistance (R) genes which mediate resistance to pathogens possessing corresponding avirulence (Avr) genes [1]. Although the protein products of Avr genes have little in common structurally, the majority of characterized R genes encode nucleotide binding leucine-rich repeat (NB-LRR) proteins (Box 1). NB-LRR-encoding genes make up one of the

A brief history of NB-LRR models

Molecular genetic studies of closely related NB-LRR proteins with differing recognition specificities indicate that the LRR domain is the primary determinant of NB-LRR protein recognition specificity 10, 11, 12, 13. Furthermore, the LRR domains of NB-LRR proteins appear to be under diversifying selection [14]. Taken together with the known role of LRR domains in protein–protein interactions, this originally led to the expectation that Avr and NB-LRR proteins might undergo receptor–ligand

The N-terminus: setting the bait

The central importance of the LRR domain in determining recognition specificity would lead to the expectation that either Avr proteins or recognition cofactors bind to this domain. At the same time, it has been generally assumed that the N-terminal domains of NB-LRR proteins function in the initiation of signaling owing to similarities in domain structure between plant NB-LRR and animal NACHT-LRR proteins 23, 24. However, all plant proteins with either confirmed or proposed roles as cofactors

From recognition to signaling: flipping the switch

If recognition involves cooperation between the LRR and N-terminal domains, what then is the nature of the mechanism or molecular switch that translates recognition into signal initiation? Structure–function analyses of the potato (Solanum tuberosum) CC-NB-LRR protein Rx indicate that this switch requires some assembly. One necessity for proper Rx function is a physical interaction between the LRR and ARC1 domains. This interaction, as well as a functional nucleotide binding pocket, is itself a

Evolutionary perspectives

All NB-LRR proteins presumably derive from a common ancestor [50], and this primordial NB-LRR protein could have functioned on the basis of either direct or indirect interaction with pathogen-derived molecules. Upon expansion of this protein family, NB-LRR proteins might have coopted various recognition cofactors which, combined with diversified LRR domains, might have offered a more complex recognition capacity. It has been suggested that a shift in recognition cofactors from guardees to

Acknowledgements

We are grateful to current and former laboratory members for stimulating discussions on NB-LRR protein function. We thank John McDowell and John Rathjen for insightful comments, suggestions and critical review of this manuscript. Work on NB-LRR proteins in the Moffett laboratory is supported by funding from the National Science Foundation (IOS-0744652) and by a National Science Foundation graduate research fellowship to S.M.C.

References (76)

  • M. Albrecht et al.

    Update on the domain architectures of NLRs and R proteins

    Biochem. Biophys. Res. Commun.

    (2006)
  • J.R. Peart

    NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus

    Curr. Biol.

    (2005)
  • D.D. Leipe

    STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer

    J. Mol. Biol.

    (2004)
  • M.J. Axtell et al.

    Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4

    Cell

    (2003)
  • J.D. Jones et al.

    The plant immune system

    Nature

    (2006)
  • M.A. Sacco et al.

    Disease resistance genes: form and function

  • A. Bendahmane

    Agrobacterium transient expression system as a tool for the isolation of disease resistance genes: application to the Rx2 locus in potato

    Plant J.

    (2000)
  • J.M. McDowell

    Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis

    Plant Cell

    (1998)
  • H. Takahashi

    RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism

    Plant J.

    (2002)
  • C.M. Tobias

    Plants expressing the Pto disease resistance gene confer resistance to recombinant PVX containing the avirulence gene AvrPto

    Plant J.

    (1999)
  • M.C. Rentel

    Recognition of the Hyaloperonospora parasitica effector ATR13 triggers resistance against oomycete, bacterial, and viral pathogens

    Proc. Natl. Acad. Sci. U. S. A.

    (2008)
  • M. Rossi

    The nematode resistance gene Mi of tomato confers resistance against the potato aphid

    Proc. Natl. Acad. Sci. U. S. A.

    (1998)
  • G. Nombela

    The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci

    Mol. Plant. Microbe Interact.

    (2003)
  • J.G. Ellis

    Further analysis of gene-for-gene disease resistance specificity in flax

    Mol. Plant Pathol.

    (2007)
  • Q.H. Shen

    Recognition specificity and RAR1/SGT1 dependence in barley Mla disease resistance genes to the powdery mildew fungus

    Plant Cell

    (2003)
  • S. Qu

    The broad-spectrum blast resistance gene Pi9 encodes a nucleotide-binding site-leucine-rich repeat protein and is a member of a multigene family in rice

    Genetics

    (2006)
  • G.J. Rairdan et al.

    Distinct domains in the ARC region of the potato resistance protein Rx mediate LRR binding and inhibition of activation

    Plant Cell

    (2006)
  • J.M. McDowell et al.

    Recent insight into R gene evolution

    Mol. Plant Pathol.

    (2006)
  • J.L. Dangl et al.

    Plant pathogens and integrated defense responses to infection

    Nature

    (2001)
  • R.A.L. van der Hoorn et al.

    From guard to decoy: a new model for perception of plant pathogen effectors

    Plant Cell

    (2008)
  • J.H. Fritz

    Nod-like proteins in immunity, inflammation and disease

    Nat. Immunol.

    (2006)
  • M.A. Sacco

    A RanGAP protein physically interacts with the NB-LRR protein Rx, and is required for Rx-mediated viral resistance

    Plant J.

    (2007)
  • X.M. Xu

    RanGAP1 is a continuous marker of the Arabidopsis cell division plane

    Proc. Natl. Acad. Sci. U. S. A.

    (2008)
  • Q.H. Shen

    Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses

    Science

    (2007)
  • G.J. Rairdan

    Novel roles for the CC and NB domains in signaling and recognition by the Rx NB-LRR disease resistance protein

    Plant Cell

    (2008)
  • P.N. Dodds

    Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes

    Proc. Natl. Acad. Sci. U. S. A.

    (2006)
  • J. Ellis

    Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions

    Annu. Rev. Phytopathol.

    (2007)
  • L. Deslandes

    Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus

    Proc. Natl. Acad. Sci. U. S. A.

    (2003)
  • Cited by (230)

    • Immune signaling networks in plant-pathogen interactions

      2023, Plant-Microbe Interaction - Recent Advances in Molecular and Biochemical Approaches: Volume 2: Agricultural Aspects of Microbiome Leading to Plant Defence
    • The role of receptor-like kinases in fungal/microbial resistance in plants

      2022, Plant Receptor-Like Kinases: Role in Development and Stress
    View all citing articles on Scopus
    View full text