Evolution of a guarded decoy protease and its receptor in solanaceous plants

Kourelis, Jiorgos ORCID: https://orcid.org/0000-0002-9007-1333, Malik, Shivani, Mattinson, Oliver, Krauter, Sonja, Kahlon, Parvinderdeep S., Paulus, Judith K. and van der Hoorn, Renier A. L. (2020) Evolution of a guarded decoy protease and its receptor in solanaceous plants. Nature Communications, 11 (1). ISSN 2041-1723

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Rcr3 is a secreted protease of tomato that is targeted by fungal effector Avr2, a secreted protease inhibitor of the fungal pathogen Cladosporium fulvum. The Avr2-Rcr3 complex is recognized by receptor-like protein Cf-2, triggering hypersensitive cell death (HR) and disease resistance. Avr2 also targets Rcr3 paralog Pip1, which is not required for Avr2 recognition but contributes to basal resistance. Thus, Rcr3 acts as a guarded decoy in this interaction, trapping the fungus into a recognition event. Here we show that Rcr3 evolved > 50 million years ago (Mya), whereas Cf-2 evolved <6Mya by co-opting the pre-existing Rcr3 in the Solanum genus. Ancient Rcr3 homologs present in tomato, potato, eggplants, pepper, petunia and tobacco can be inhibited by Avr2 with the exception of tobacco Rcr3. Four variant residues in Rcr3 promote Avr2 inhibition, but the Rcr3 that co-evolved with Cf-2 lacks three of these residues, indicating that the Rcr3 co-receptor is suboptimal for Avr2 binding. Pepper Rcr3 triggers HR with Cf-2 and Avr2 when engineered for enhanced inhibition by Avr2. Nicotiana benthamiana (Nb) is a natural null mutant carrying Rcr3 and Pip1 alleles with deleterious frame-shift mutations. Resurrected NbRcr3 and NbPip1 alleles were active proteases and further NbRcr3 engineering facilitated Avr2 inhibition, uncoupled from HR signalling. The evolution of a receptor co-opting a conserved pathogen target contrasts with other indirect pathogen recognition mechanisms.

Item Type: Article
Additional Information: Acknowledgements: The authors thank Matthieu Joosten for sending the Cf-2::EGFP and Cf-4::EGFP plasmids; the ENSA consortium for providing general Golden Gate-compatible plasmids; Ursula Pyzio for excellent plant care; John Baker for photography; Jonathan Jones, Sophien Kamoun, James Carrington, Sylvestre Marillonnet, and Nicola Patron for providing plasmids via AddGene. This work has been supported by ‘The Clarendon Fund’ (JK), the Oxford Indira Gandhi Graduate Scholarship (SM), ERC Consolidator grant 616449 ‘Green-Proteases’ (RvdH, JK), and BBSRC grant BB/S003193/1 ‘Pip1S’ (RH). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Data availability: All data supporting the findings of this study are available in the manuscript and its supplementary files. The data underlying Figs. 2c, 3f, 5a, 6a–d and Supplementary Figs. 5 and 6a, b are provided as a Source File. All alignments (fasta files) and trees (newick files) have been deposited on Oxford Research Archive at https://doi.org/10.5287/bodleian:VJwe6gBNx. Phylogenetics trees of Figs. 3g, 4a, 7, S2, S4, S7, S8 can also be viewed on iTOL (https://itol.embl.de/shared/JKourelis). Source data are provided with this paper.
Uncontrolled Keywords: chemistry(all),biochemistry, genetics and molecular biology(all),physics and astronomy(all) ,/dk/atira/pure/subjectarea/asjc/1600
Faculty \ School: Faculty of Science > The Sainsbury Laboratory
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Depositing User: LivePure Connector
Date Deposited: 07 Dec 2023 01:45
Last Modified: 01 Feb 2024 03:07
URI: https://ueaeprints.uea.ac.uk/id/eprint/93889
DOI: 10.1038/s41467-020-18069-5

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