title: Functional Divergence of Two Secreted Immune Proteases of Tomato.
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. 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.
authors: Plant Chemetics Laboratory, Max Planck Institute for Plant Breeding Research, Carl-von-Linné Weg 10, 50829 Cologne, Germany.
authors: Muhammad
authors: M
authors: Ilyas
authors: Plant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB Oxford, UK; Plant Chemetics Laboratory, Max Planck Institute for Plant Breeding Research, Carl-von-Linné Weg 10, 50829 Cologne, Germany.
authors: Anja C
authors: AC
authors: Hörger
authors: The Sainsbury Laboratory, Norwich Research Park, NR4 7UH Norwich, UK.
authors: Tolga O
authors: TO
authors: Bozkurt
authors: Molecular Plant Pathology, Swammerdam Institute for Life Sciences, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, the Netherlands.
authors: Harrold A
authors: HA
authors: van den Burg
authors: Chemical Biology, Fakultät für Biologie, Zentrum für Medizinische Biotechnologie, Universität Duisburg-Essen, Universitätstr. 2, 45117 Essen, Germany.
authors: Farnusch
authors: F
authors: Kaschani
authors: Chemical Biology, Fakultät für Biologie, Zentrum für Medizinische Biotechnologie, Universität Duisburg-Essen, Universitätstr. 2, 45117 Essen, Germany.
authors: Markus
authors: M
authors: Kaiser
authors: The Sainsbury Laboratory, Norwich Research Park, NR4 7UH Norwich, UK.
authors: Khaoula
authors: K
authors: Belhaj
authors: The Sainsbury Laboratory, Norwich Research Park, NR4 7UH Norwich, UK.
authors: Matthew
authors: M
authors: Smoker
authors: SOL Group, Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, the Netherlands.
authors: Matthieu H A J
authors: MH
authors: Joosten
authors: The Sainsbury Laboratory, Norwich Research Park, NR4 7UH Norwich, UK.
authors: Sophien
authors: S
authors: Kamoun
authors: Plant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB Oxford, UK; Plant Chemetics Laboratory, Max Planck Institute for Plant Breeding Research, Carl-von-Linné Weg 10, 50829 Cologne, Germany. Electronic address: renier.vanderhoorn@plants.ox.ac.uk.
authors: Renier A L
authors: RA
authors: van der Hoorn
mesh_terms: D002963:Cladosporium / Q000502:physiology*; D019143:Evolution, Molecular; D020440:Gene Duplication; D018551:Solanum lycopersicum / Q000235:genetics* / Q000276:immunology / Q000378:metabolism; D010447:Peptide Hydrolases / Q000235:genetics* / Q000378:metabolism; D055750:Phytophthora infestans / Q000502:physiology*; D010940:Plant Proteins / Q000235:genetics* / Q000378:metabolism
chemical_list: D010940:Plant Proteins; D010447:Peptide Hydrolases
keywords: Cladosporium fulvum; Cys protease; Phytophthora infestans; apoplast; immunity; tomato