Structurally distinct Arabidopsis thaliana NLR immune receptors recognize tandem WY domains of an oomycete effector

New Phytol. 2016 May;210(3):984-96. doi: 10.1111/nph.13823. Epub 2016 Jan 4.

Abstract

Nucleotide-binding leucine-rich repeat (NB-LRR, or NLR) receptors mediate pathogen recognition. The Arabidopsis thaliana NLR RPP1 recognizes the tandem WY-domain effector ATR1 from the oomycete Hyaloperonospora arabidopsidis through direct association with C-terminal LRRs. We isolated and characterized homologous NLR genes RPP1-EstA and RPP1-ZdrA from two Arabidopsis ecotypes, Estland (Est-1) and Zdarec (Zdr-1), responsible for recognizing a novel spectrum of ATR1 alleles. RPP1-EstA and -ZdrA encode nearly identical NLRs that are phylogenetically distinct from known immunity-activating RPP1 homologs and possess greatly expanded LRR domains. Site-directed mutagenesis and truncation analysis of ATR1 suggests that these homologs recognize a novel surface of the 2(nd) WY domain of ATR1, partially specified by a C-terminal region of the LRR domain. Synteny comparison with RPP1 loci involved in hybrid incompatibility suggests that these functions evolved independently. Closely related RPP1 homologs have diversified their recognition spectra through LRR expansion and sequence variation, allowing them to detect multiple surfaces of the same pathogen effector. Engineering NLR receptor specificity may require a similar combination of repeat expansion and tailored amino acid variation.

Keywords: ATR1; Estland (Est-1); Hyaloperonospora arabidopsidis; RPP1; Zdarec (Zdr-1); nucleotide binding-leucine rich repeat receptor (NLR); plant immunity; resistance protein.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Alleles
  • Amino Acid Sequence
  • Arabidopsis / immunology*
  • Arabidopsis / microbiology*
  • Arabidopsis Proteins / chemistry*
  • Arabidopsis Proteins / metabolism*
  • Chromosome Segregation
  • Crosses, Genetic
  • Ecotype
  • Genetic Loci
  • Genome, Plant
  • Molecular Sequence Annotation
  • Oomycetes / physiology*
  • Phenotype
  • Phylogeny
  • Polymorphism, Genetic
  • Protein Domains
  • Proteins / chemistry*
  • Proteins / metabolism*
  • Receptors, Cell Surface / chemistry
  • Receptors, Cell Surface / metabolism
  • Sequence Homology, Amino Acid

Substances

  • Arabidopsis Proteins
  • Proteins
  • Receptors, Cell Surface
  • leucine-rich repeat proteins

Associated data

  • GENBANK/KT722749
  • GENBANK/KT722750
  • GENBANK/KT722751
  • GENBANK/KT722752