Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Analysis of intraspecies diversity reveals a subset of highly variable plant immune receptors and predicts their binding sites

Journal Article · · Plant Cell
 [1];  [2]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Univ. of California, Berkeley, CA (United States)
The evolution of recognition specificities by the immune system depends on the generation of receptor diversity and on connecting the binding of new antigens with the initiation of downstream signaling. In plant immunity, the innate Nucleotide-Binding Leucine-Rich Repeat (NLR) receptor family enables antigen binding and immune signaling. In this study, we surveyed the NLR complements of 62 ecotypes of Arabidopsis thaliana and 54 lines of Brachypodium distachyon and identified a limited number of NLR subfamilies that show high allelic diversity. We show that the predicted specificity-determining residues cluster on the surfaces of Leucine-Rich Repeat domains, but the locations of the clusters vary among NLR subfamilies. By comparing NLR phylogeny, allelic diversity, and known functions of the Arabidopsis NLRs, we formulate a hypothesis for the emergence of direct and indirect pathogen-sensing receptors and of the autoimmune NLRs. These findings reveal the recurring patterns of evolution of innate immunity and can inform NLR engineering efforts.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); Gordon and Betty Moore Foundation; Foundation for Food and Agriculture Research
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1825905
Journal Information:
Plant Cell, Journal Name: Plant Cell Journal Issue: 4 Vol. 33; ISSN 1040-4651
Publisher:
American Society of Plant BiologistsCopyright Statement
Country of Publication:
United States
Language:
English

References (62)

UCSF Chimera?A visualization system for exploratory research and analysis journal January 2004
Information-theoretical entropy as a measure of sequence variability journal December 1991
The relationship of leaf rust resistance gene Lr13 and hybrid necrosis gene Ne2m on wheat chromosome 2BS journal December 2015
Contrasting patterns of evolution between allelic groups at a single locus in Arabidopsis journal August 2006
A Shannon entropy analysis of immunoglobulin and T cell receptor journal October 1997
Species-wide Genetic Incompatibility Analysis Identifies Immune Genes as Hot Spots of Deleterious Epistasis journal December 2014
A Species-Wide Inventory of NLR Genes and Alleles in Arabidopsis thaliana journal August 2019
Unusual signatures of highly adaptable R-loci in closely-related Arabidopsis species journal August 2011
Automated subtyping of HIV-1 genetic sequences for clinical and surveillance purposes: Performance evaluation of the new REGA version 3 and seven other tools journal October 2013
NLR diversity, helpers and integrated domains: making sense of the NLR IDentity journal August 2017
Help wanted: helper NLRs and plant immune responses journal August 2019
The Phyre2 web portal for protein modeling, prediction and analysis journal May 2015
Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure journal December 2017
The Cf-2 / Rcr3esc gene interaction in tomato (Lycopersicon esculentum) induces autonecrosis and triggers biochemical markers of oxidative burst at cellular level journal January 2003
Recognition of the Hyaloperonospora parasitica effector ATR13 triggers resistance against oomycete, bacterial, and viral pathogens journal January 2008
Organization of lamprey variable lymphocyte receptor C locus and repertoire development journal March 2013
Rapidly evolving R genes in diverse grass species confer resistance to rice blast disease journal October 2013
NLR network mediates immunity to diverse plant pathogens journal July 2017
RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference journal May 2019
PAML 4: Phylogenetic Analysis by Maximum Likelihood journal April 2007
Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions journal April 2013
Interactive Tree Of Life (iTOL) v4: recent updates and new developments journal April 2019
Protein sequence entropy is closely related to packing density and hydrophobicity journal February 2005
The Major Specificity-Determining Amino Acids of the Tomato Cf-9 Disease Resistance Protein Are at Hypervariable Solvent-Exposed Positions in the Central Leucine-Rich Repeats journal October 2009
The AvrM Effector from Flax Rust Has a Structured C-Terminal Domain and Interacts Directly with the M Resistance Protein journal January 2010
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes journal September 2003
Clusters of Resistance Genes in Plants Evolve by Divergent Selection and a Birth-and-Death Process journal November 1998
Large-Scale Analyses of Angiosperm Nucleotide-Binding Site-Leucine-Rich Repeat Genes Reveal Three Anciently Diverged Classes with Distinct Evolutionary Patterns journal February 2016
NLR Mutations Suppressing Immune Hybrid Incompatibility and Their Effects on Disease Resistance journal May 2018
Multiple Genetic Processes Result in Heterogeneous Rates of Evolution within the Major Cluster Disease Resistance Genes in Lettuce[W] journal November 2004
Differential Recognition of Highly Divergent Downy Mildew Avirulence Gene Alleles by RPP1 Resistance Genes from Two Arabidopsis Lines journal May 2005
A Genome-Wide Survey of R Gene Polymorphisms in Arabidopsis journal June 2006
Activation of an Arabidopsis Resistance Protein Is Specified by the in Planta Association of Its Leucine-Rich Repeat Domain with the Cognate Oomycete Effector journal July 2010
Heterogeneity and Structure of Antibody-Combining Sites journal February 1970
Structurally distinct Arabidopsis thaliana NLR immune receptors recognize tandem WY domains of an oomycete effector journal January 2016
Multiple strategies for pathogen perception by plant immune receptors journal November 2017
Subsets of NLR genes show differential signatures of adaptation during colonization of new habitats journal June 2019
Evolution of NLR resistance genes with noncanonical N‐terminal domains in wild tomato species journal May 2020
A Tomato Cysteine Protease Required for Cf-2 -Dependent Disease Resistance and Suppression of Autonecrosis journal April 2002
Antigen Recognition by Variable Lymphocyte Receptors journal September 2008
Pivoting the Plant Immune System from Dissection to Deployment journal August 2013
Intracellular innate immune surveillance devices in plants and animals journal December 2016
Loss of AvrSr50 by somatic exchange in stem rust leads to virulence for Sr50 resistance in wheat journal December 2017
Ligand-triggered allosteric ADP release primes a plant NLR complex journal April 2019
Reconstitution and structure of a plant NLR resistosome conferring immunity journal April 2019
Structure of the activated ROQ1 resistosome directly recognizing the pathogen effector XopQ journal December 2020
Direct pathogen-induced assembly of an NLR immune receptor complex to form a holoenzyme journal December 2020
Too much of a good thing? Hybrid necrosis as a by-product of plant immune system diversification journal November 2009
Evolution of Plant NLRs: From Natural History to Precise Modifications journal April 2020
Flax Rust Resistance Gene Specificity is Based on Direct Resistance-Avirulence Protein Interactions journal September 2007
ss-TEA: Entropy based identification of receptor specific ligand binding residues from a multiple sequence alignment of class A GPCRs journal August 2011
Sequence variation in ligand binding sites in proteins journal September 2005
Selection in the evolution of gene duplications journal January 2002
TNL genes in peach: insights into the post-LRR domain journal April 2016
Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens journal February 2016
Dominant integration locus drives continuous diversification of plant immune receptors with exogenous domain fusions journal February 2018
Autoimmune Response as a Mechanism for a Dobzhansky-Muller-Type Incompatibility Syndrome in Plants journal September 2007
Structural Consensus among Antibodies Defines the Antigen Binding Site journal February 2012
The de Novo Reference Genome and Transcriptome Assemblies of the Wild Tomato Species Solanum chilense Highlights Birth and Death of NLR Genes Between Tomato Species journal December 2019
The Maintenance of Extreme Amino Acid Diversity at the Disease Resistance Gene, RPP13 , in Arabidopsis thaliana journal March 2004
LRRpredictor—A New LRR Motif Detection Method for Irregular Motifs of Plant NLR Proteins Using an Ensemble of Classifiers journal March 2020
Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism journal February 2019

Similar Records

High allelic diversity in Arabidopsis NLRs is associated with distinct genomic features
Journal Article · Mon Mar 25 00:00:00 EDT 2024 · EMBO Reports · OSTI ID:2470735

The structural basis of flagellin detection by NAIP5: A strategy to limit pathogen immune evasion
Journal Article · Wed Nov 15 23:00:00 EST 2017 · Science · OSTI ID:1524058

The N-terminal domains of NLR immune receptors exhibit structural and functional similarities across divergent plant lineages
Journal Article · Wed Apr 10 00:00:00 EDT 2024 · The Plant Cell · OSTI ID:2471114

Related Subjects