Mechanisms of RALF peptide perception by a heterotypic receptor complex

Nature. 2019 Aug;572(7768):270-274. doi: 10.1038/s41586-019-1409-7. Epub 2019 Jul 10.

Abstract

Receptor kinases of the Catharanthus roseus RLK1-like (CrRLK1L) family have emerged as important regulators of plant reproduction, growth and responses to the environment1. Endogenous RAPID ALKALINIZATION FACTOR (RALF) peptides2 have previously been proposed as ligands for several members of the CrRLK1L family1. However, the mechanistic basis of this perception is unknown. Here we report that RALF23 induces a complex between the CrRLK1L FERONIA (FER) and LORELEI (LRE)-LIKE GLYCOSYLPHOSPHATIDYLINOSITOL (GPI)-ANCHORED PROTEIN 1 (LLG1) to regulate immune signalling. Structural and biochemical data indicate that LLG1 (which is genetically important for RALF23 responses) and the related LLG2 directly bind RALF23 to nucleate the assembly of RALF23-LLG1-FER and RALF23-LLG2-FER heterocomplexes, respectively. A conserved N-terminal region of RALF23 is sufficient for the biochemical recognition of RALF23 by LLG1, LLG2 or LLG3, and binding assays suggest that other RALF peptides that share this conserved N-terminal region may be perceived by LLG proteins in a similar manner. Structural data also show that RALF23 recognition is governed by the conformationally flexible C-terminal sides of LLG1, LLG2 and LLG3. Our work reveals a mechanism of peptide perception in plants by GPI-anchored proteins that act together with a phylogenetically unrelated receptor kinase. This provides a molecular framework for understanding how diverse RALF peptides may regulate multiple processes, through perception by distinct heterocomplexes of CrRLK1L receptor kinases and GPI-anchored proteins of the LRE and LLG family.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / immunology*
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / chemistry*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • GPI-Linked Proteins / metabolism*
  • Intercellular Signaling Peptides and Proteins / chemistry*
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / metabolism*
  • Models, Molecular
  • Mutagenesis
  • Mutant Proteins / chemistry
  • Mutant Proteins / genetics
  • Mutant Proteins / metabolism
  • Mutation
  • Peptide Fragments / chemistry
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism*
  • Phosphotransferases / genetics
  • Phosphotransferases / metabolism*
  • Pliability
  • Protein Binding / genetics
  • Protein Conformation
  • Protein Multimerization

Substances

  • AT2G20700 protein, Arabidopsis
  • AT3G16570 protein, Arabidopsis
  • AT4G28280 protein, Arabidopsis
  • Arabidopsis Proteins
  • GPI-Linked Proteins
  • Intercellular Signaling Peptides and Proteins
  • LLG1 protein, Arabidopsis
  • Mutant Proteins
  • Peptide Fragments
  • FERONIA receptor like kinase, Arabidopsis
  • Phosphotransferases