Functional Divergence of Two Secreted Immune Proteases of Tomato

Muhammad Ilyas, Anja C. Hörger, Tolga O. Bozkurt, Harrold A. Van Den Burg, Farnusch Kaschani, Markus Kaiser, Khaoula Belhaj, Matthew Smoker, Matthieu H A J Joosten, Sophien Kamoun, Renier A L Van Der Hoorn

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39 Citations (Scopus)

Abstract

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 [1-4]. 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.

Original languageEnglish
Pages (from-to)2300-2306
Number of pages7
JournalCurrent Biology
Volume25
Issue number17
DOIs
Publication statusPublished - Aug 2015

Keywords

  • apoplast
  • Cladosporium fulvum
  • Cys protease
  • immunity
  • Phytophthora infestans
  • tomato

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