Functional Divergence of Two Secreted Immune Proteases of Tomato

Curr Biol. 2015 Aug 31;25(17):2300-6. doi: 10.1016/j.cub.2015.07.030. Epub 2015 Aug 20.


Rcr3 and Pip1 are paralogous secreted papain-like proteases of tomato. Both proteases are inhibited by Avr2 from the fungal pathogen Cladosporium fulvum, but only Rcr3 acts as a co-receptor for Avr2 recognition by the tomato Cf-2 immune receptor. Here, we show that Pip1-depleted tomato plants are hyper-susceptible to fungal, bacterial, and oomycete plant pathogens, demonstrating that Pip1 is an important broad-range immune protease. By contrast, in the absence of Cf-2, Rcr3 depletion does not affect fungal and bacterial infection levels but causes increased susceptibility only to the oomycete pathogen Phytophthora infestans. Rcr3 and Pip1 reside on a genetic locus that evolved over 36 million years ago. These proteins differ in surface-exposed residues outside the substrate-binding groove, and Pip1 is 5- to 10-fold more abundant than Rcr3. We propose a model in which Rcr3 and Pip1 diverged functionally upon gene duplication, possibly driven by an arms race with pathogen-derived inhibitors or by coevolution with the Cf-2 immune receptor detecting inhibitors of Rcr3, but not of Pip1.

Keywords: Cladosporium fulvum; Cys protease; Phytophthora infestans; apoplast; immunity; tomato.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cladosporium / physiology*
  • Evolution, Molecular*
  • Gene Duplication
  • Peptide Hydrolases / genetics*
  • Peptide Hydrolases / metabolism
  • Phytophthora infestans / physiology*
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Solanum lycopersicum / genetics*
  • Solanum lycopersicum / immunology
  • Solanum lycopersicum / metabolism


  • Plant Proteins
  • Peptide Hydrolases