Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence

Cell Res. 2011 May;21(5):835-48. doi: 10.1038/cr.2011.4. Epub 2011 Jan 11.

Abstract

Emerging evidence suggests that E3 ligases play critical roles in diverse biological processes, including innate immune responses in plants. However, the mechanism of the E3 ligase involvement in plant innate immunity is unclear. We report that a rice gene, OsBBI1, encoding a RING finger protein with E3 ligase activity, mediates broad-spectrum disease resistance. The expression of OsBBI1 was induced by rice blast fungus Magnaporthe oryzae, as well as chemical inducers, benzothiadiazole and salicylic acid. Biochemical analysis revealed that OsBBI1 protein possesses E3 ubiquitin ligase activity in vitro. Genetic analysis revealed that the loss of OsBBI1 function in a Tos17-insertion line increased susceptibility, while the overexpression of OsBBI1 in transgenic plants conferred enhanced resistance to multiple races of M. oryzae. This indicates that OsBBI1 modulates broad-spectrum resistance against the blast fungus. The OsBBI1-overexpressing plants showed higher levels of H(2)O(2) accumulation in cells and higher levels of phenolic compounds and cross-linking of proteins in cell walls at infection sites by M. oryzae compared with wild-type (WT) plants. The cell walls were thicker in the OsBBI1-overexpressing plants and thinner in the mutant plants than in the WT plants. Our results suggest that OsBBI1 modulates broad-spectrum resistance to blast fungus by modifying cell wall defence responses. The functional characterization of OsBBI1 provides insight into the E3 ligase-mediated innate immunity, and a practical tool for constructing broad-spectrum resistance against the most destructive disease in rice.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Cell Wall / drug effects
  • Cell Wall / immunology*
  • Cell Wall / microbiology
  • Cell Wall / ultrastructure
  • Hydrogen Peroxide / metabolism
  • Immunity, Innate*
  • Magnaporthe / drug effects
  • Magnaporthe / physiology*
  • Molecular Sequence Data
  • Mutation / genetics
  • Phenols / metabolism
  • Plant Diseases / immunology*
  • Plant Diseases / microbiology*
  • Plant Epidermis / cytology
  • Plant Epidermis / metabolism
  • Plant Epidermis / microbiology
  • Plant Epidermis / ultrastructure
  • Plant Proteins / chemistry
  • Plant Proteins / metabolism*
  • Salicylic Acid / pharmacology
  • Sequence Alignment
  • Thiadiazoles / pharmacology
  • Ubiquitin-Protein Ligases / metabolism*

Substances

  • Phenols
  • Plant Proteins
  • Thiadiazoles
  • benzo-1,2,3-thiadiazole
  • Hydrogen Peroxide
  • Ubiquitin-Protein Ligases
  • Salicylic Acid