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

Functional Divergence of Two Secreted Immune Proteases of Tomato.

Author information

1
Plant Chemetics Laboratory, Max Planck Institute for Plant Breeding Research, Carl-von-Linné Weg 10, 50829 Cologne, Germany.
2
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.
3
The Sainsbury Laboratory, Norwich Research Park, NR4 7UH Norwich, UK.
4
Molecular Plant Pathology, Swammerdam Institute for Life Sciences, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, the Netherlands.
5
Chemical Biology, Fakultät für Biologie, Zentrum für Medizinische Biotechnologie, Universität Duisburg-Essen, Universitätstr. 2, 45117 Essen, Germany.
6
SOL Group, Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, the Netherlands.
7
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.

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.

KEYWORDS:

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

PMID:
26299516
DOI:
10.1016/j.cub.2015.07.030
[Indexed for MEDLINE]
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