Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor

Proc Natl Acad Sci U S A. 2019 Apr 23;116(17):8525-8534. doi: 10.1073/pnas.1818275116. Epub 2019 Apr 4.

Abstract

The rice immune receptor XA21 is activated by the sulfated microbial peptide required for activation of XA21-mediated immunity X (RaxX) produced by Xanthomonas oryzae pv. oryzae (Xoo). Mutational studies and targeted proteomics revealed that the RaxX precursor peptide (proRaxX) is processed and secreted by the protease/transporter RaxB, the function of which can be partially fulfilled by a noncognate peptidase-containing transporter component B (PctB). proRaxX is cleaved at a Gly-Gly motif, yielding a mature peptide that retains the necessary elements for RaxX function as an immunogen and host peptide hormone mimic. These results indicate that RaxX is a prokaryotic member of a previously unclassified and understudied group of eukaryotic tyrosine sulfated ribosomally synthesized, posttranslationally modified peptides (RiPPs). We further demonstrate that sulfated RaxX directly binds XA21 with high affinity. This work reveals a complete, previously uncharacterized biological process: bacterial RiPP biosynthesis, secretion, binding to a eukaryotic receptor, and triggering of a robust host immune response.

Keywords: ABC transporter; RIPP; immunogen; peptidase; sulfation.

Publication types

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

MeSH terms

  • ATP-Binding Cassette Transporters / chemistry
  • ATP-Binding Cassette Transporters / genetics
  • ATP-Binding Cassette Transporters / metabolism
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Genes, Bacterial / genetics
  • Host-Pathogen Interactions / genetics
  • Host-Pathogen Interactions / immunology
  • Metabolic Networks and Pathways / genetics
  • Oryza / immunology
  • Oryza / metabolism
  • Oryza / microbiology
  • Peptide Hydrolases / chemistry
  • Peptide Hydrolases / genetics
  • Peptide Hydrolases / metabolism*
  • Peptides / chemistry
  • Peptides / genetics
  • Peptides / metabolism*
  • Plant Proteins / chemistry
  • Plant Proteins / immunology
  • Plant Proteins / metabolism*
  • Protein-Serine-Threonine Kinases / chemistry
  • Protein-Serine-Threonine Kinases / immunology
  • Protein-Serine-Threonine Kinases / metabolism*
  • Xanthomonas / genetics
  • Xanthomonas / metabolism
  • Xanthomonas / pathogenicity

Substances

  • ATP-Binding Cassette Transporters
  • Bacterial Proteins
  • Peptides
  • Plant Proteins
  • Xa21 protein, Oryza sativa
  • Protein-Serine-Threonine Kinases
  • Peptide Hydrolases