Variation and inheritance of the Xanthomonas raxX-raxSTAB gene cluster required for activation of XA21-mediated immunity

Mol Plant Pathol. 2019 May;20(5):656-672. doi: 10.1111/mpp.12783. Epub 2019 Feb 18.

Abstract

The rice XA21-mediated immune response is activated on recognition of the RaxX peptide produced by the bacterium Xanthomonas oryzae pv. oryzae (Xoo). The 60-residue RaxX precursor is post-translationally modified to form a sulfated tyrosine peptide that shares sequence and functional similarity with the plant sulfated tyrosine (PSY) peptide hormones. The 5-kb raxX-raxSTAB gene cluster of Xoo encodes RaxX, the RaxST tyrosylprotein sulfotransferase, and the RaxA and RaxB components of a predicted type I secretion system. To assess raxX-raxSTAB gene cluster evolution and to determine its phylogenetic distribution, we first identified rax gene homologues in other genomes. We detected the complete raxX-raxSTAB gene cluster only in Xanthomonas spp., in five distinct lineages in addition to X. oryzae. The phylogenetic distribution of the raxX-raxSTAB gene cluster is consistent with the occurrence of multiple lateral (horizontal) gene transfer events during Xanthomonas speciation. RaxX natural variants contain a restricted set of missense substitutions, as expected if selection acts to maintain peptide hormone-like function. Indeed, eight RaxX variants tested all failed to activate the XA21-mediated immune response, yet retained peptide hormone activity. Together, these observations support the hypothesis that the XA21 receptor evolved specifically to recognize Xoo RaxX.

Keywords: XA21; Xoo; plant immunity; raxX-raxSTAB gene cluster.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Sequence
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Conserved Sequence
  • Gene Transfer, Horizontal / genetics
  • Genome, Bacterial
  • Inheritance Patterns / genetics*
  • Multigene Family*
  • Mutation, Missense / genetics
  • Oryza / immunology*
  • Oryza / microbiology*
  • Phylogeny
  • Plant Immunity / genetics*
  • Plant Proteins / metabolism*
  • Plant Roots / growth & development
  • Plant Roots / microbiology
  • Protein Serine-Threonine Kinases / metabolism*
  • Recombination, Genetic / genetics
  • Xanthomonas / genetics*

Substances

  • Bacterial Proteins
  • Plant Proteins
  • Xa21 protein, Oryza sativa
  • Protein Serine-Threonine Kinases